Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils
Open accessAbstract
Cyanobacteria are among the most ancient of evolutionary lineages, oxygenic photosynthesizers that may have originated before 3.0 Ga, as evidenced by free oxygen levels. Throughout the P recambrian, cyanobacteria were one of the most important drivers of biological innovations, strongly impacting early Earth's environments. At the end of the A rchean E on, they were responsible for the rapid oxygenation of Earth's atmosphere during an episode referred to as the G reat O xidation E vent (GOE). However, little is known about the origin and diversity of early cyanobacterial taxa, due to: (1) the scarceness of P recambrian fossil deposits; (2) limited characteristics for the identification of taxa; and (3) the poor preservation of ancient microfossils. Previous studies based on 16 S r RNA have suggested that the origin of multicellularity within cyanobacteria might have been associated with the GOE. However, single‐gene analyses have limitations, particularly for deep branches. We reconstructed the evolutionary history of cyanobacteria using genome scale data and re‐evaluated the P recambrian fossil record to get more precise calibrations for a relaxed clock analysis. For the phylogenomic reconstructions, we identified 756 conserved gene sequences in 65 cyanobacterial taxa, of which eight genomes have been sequenced in this study. Character state reconstructions based on maximum likelihood and Bayesian phylogenetic inference confirm previous findings, of an ancient multicellular cyanobacterial lineage ancestral to the majority of modern cyanobacteria. Relaxed clock analyses provide firm support for an origin of cyanobacteria in the A rchean and a transition to multicellularity before the GOE. It is likely that multicellularity had a greater impact on cyanobacterial fitness and thus abundance, than previously assumed. Multicellularity, as a major evolutionary innovation, forming a novel unit for selection to act upon, may have served to overcome evolutionary constraints and enabled diversification of the variety of morphotypes seen in cyanobacteria today.
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TL;DR
Genome-scale phylogenomics and relaxed molecular clock analyses of 65 cyanobacterial taxa support an Archean origin of cyanobacteria and an origin of multicellularity before the Great Oxidation Event, with multicellularity later lost and occasionally regained. The authors argue this early multicellularity may have increased cyanobacterial abundance and oxygen production, contributing to the GOE.
Key findings
- The phylogenomic tree, based on 756 conserved proteins (197,761 amino acid sites) from 65 cyanobacterial taxa, recovered six major clades with full bootstrap support; 100% maximum likelihood bootstrap support was inferred for 57 of 64 branches, compared with 24 of 64 branches in the 16S/23S rRNA tree.
- Ancestral character state reconstruction inferred a very early transition to multicellularity at node/branch 69; multicellularity was subsequently lost at least five times and regained on one, possibly two, branches leading to *Leptolyngbya* sp. PCC 7376 and *Spirulina subsalsa* PCC 9445, so the majority of modern cyanobacteria are descendants of an ancient multicellular lineage.
- Relaxed clock analyses, irrespective of prior assumptions for node 69, estimated that multicellularity originated before the GOE; cyanobacteria originated in the Archean/mid-Archean long before the GOE, and the majority of modern clades 2–6 evolved after the GOE.
- Comparisons of modern cyanobacterial cell sizes to Precambrian microfossils support the inferred presence of multicellular cyanobacteria before the GOE, but the fossil record does not provide evidence for multicellular taxa among the earliest unequivocal fossil assemblages at 3.33–3.45 Ga.
Methods
- Taxon sampling and phylogenomics: 65 cyanobacterial taxa were analyzed, including 27 unicellular (sections I–II) and 38 multicellular (sections III–V) taxa; eight additional cyanobacterial genomes were sequenced. A total of 756 highly conserved proteins were identified, aligned, and concatenated into a 197,761-amino-acid supermatrix; maximum likelihood trees were reconstructed with RAxML using the LG + Γ model and 1000 bootstrap resamplings, alongside a concatenated 16S/23S rRNA tree.
- Ancestral character state reconstruction: maximum likelihood methods in the R ape package and Bayesian inference in BayesTraits were used; MCMC analyses ran for 1,010,000 iterations with a 10,000 burn-in, estimating transition rates q01 (to multicellularity) and q10 (to unicellularity).
- Divergence time estimation: relaxed clocks with lognormal rate distribution were applied in MCMCTREE/PAML, using three calibrations—origin of Cyanobacteria, origin of sections IV and V capable of cellular differentiation, and origin of multicellularity at node 69. Two hypotheses were tested: multicellularity after the GOE (H1) versus before the GOE (H2); four MCMC analyses ran for 10 million generations, sampling every 100 generations with 50% burn-in.
Limitations
- Stated: deep divergences are limited by the lack of evolutionary information retained in molecular data over long timescales, weaknesses in phylogenetic models, paucity of calibration points, potential misassignment of calibrations, and the likelihood that fossil ages poorly approximate clade ages; posterior node age estimates had large 95% confidence intervals that prevented precise dating.
- Stated: the Precambrian fossil record is patchy at best; the earliest unequivocal fossil assemblages at 3.33–3.45 Ga do not provide evidence for multicellular cyanobacteria, and filament diameters in older fossils are described as “more probabilistic than deterministic” evidence for cyanobacteria.
- Evident from the text: the analyses depend on debated fossil interpretations and geochemical inferences for calibration, use only uniform prior distributions, and showed that user-specified priors can differ from effective priors, although the authors judged the age ranges similar enough to accept.
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Claims the paper makes
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- Findingown data
Relaxed clock analyses provide firm support for an origin of cyanobacteria in the Archean.
“Relaxed clock analyses provide firm support for an origin of cyanobacteria in the Archean and a transition to multicellularity before the GOE.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The divergence of the Gloeobacter lineage from the stem lineage leading to all other extant cyanobacteria occurred between 3.85 and 2.918 Ga (analyses A, C) or between 3.85 and 2.45 Ga (analyses B, D).
- Findingown data
Relaxed clock analyses provide firm support for a transition to multicellularity before the GOE.
“Relaxed clock analyses provide firm support for an origin of cyanobacteria in the Archean and a transition to multicellularity before the GOE.”
Quote in the paperSubstantial claim- The authors state this as an assumption: The most recent common ancestor of subsections IV and V cyanobacteria originated after the GOE but before 1.957 Ga.
- Findingown data
Results of all analyses suggest a very early transition to multicellularity at node/branch 69.
“Results of all analyses suggest a very early transition to multicellularity at ‘node/branch 69’ (Fig. 3; Fig. S3; Table S3).”
Quote in the paperSubstantial claim - Findingown data
Changing the widths of the uniform distribution in several runs supported an early transition to multicellularity even further.
“Changing the widths of the uniform distribution in several runs supported an early transition to multicellularity even further (Fig. S3, online Supporting Information).”
Quote in the paperNot a substantial claim - Findingreasoning
Synechococcus isolated from hot springs are the first group to split from the rest of Cyanobacteria.
“Assuming that Gloeobacter groups closest to a eubacterial outgroup, as previously suggested based on ribosomal (Schirrmeister et al. 2011b), and phylogenomic data (Blank and Sanchez‐Baracaldo 2010; Shih et al. 2013), Synechococcus isolated from hot springs are the first group to split from the rest of Cyanobacteria, followed by an early branching ‘Clade 1’ of unicellular and multicellular cyan”
Quote in the paperNot a substantial claim
- Findingown data
Analyses run without molecular data showed that originally uniform priors resulted in non-uniform effective priors.
“Our analyses run without molecular data showed that our originally uniform priors (Fig. 4; dashed curve) resulted in non‐uniform effective priors (Fig. 4; red curve).”
Quote in the paperSubstantial claim - Findingown data
For character state reconstructions using an asymmetrical rate model, the estimated rates were q01 = 0.5768 (standard error = 0.3147) and q10 = 0.8254 (standard error = 0.2205).
“For character state reconstructions using an asymmetrical rate model, the estimated rates were q01 = 0.5768 (standard error = 0.3147) and q10 = 0.8254 (standard error = 0.2205), where q01 defines the transition to multicellularity and q01 the loss of multicellularity.”
Quote in the paperSubstantial claim - Findingown data
Six distinct clades could be reconstructed with full support.
“Six distinct clades could be reconstructed with full support.”
Quote in the paperNot a substantial claim - Findingown data
In all analyses, the posterior probabilities of the origin of multicellularity support an age close to the maximum of the prior age calibration.
“In all analyses, the posterior probabilities of the origin of multicellularity (calibration 3; Fig. 4) support an age close to the maximum of the prior age calibration.”
Quote in the paperNot a substantial claim - Findingown data
The posterior age estimates for the origin of multicellularity are in all cases shifted towards the older bound of the effective priors.
“The posterior age estimates for the origin of multicellularity (calibration 3) are in all cases shifted towards the older bound of the effective priors.”
Quote in the paperNot a substantial claim - Findingown data
Several genera appear polyphyletic, such as Synechococcus, Geitlerinema and Pseudanabaena.
“Several forms of genera appear polyphyletic, such as Synechococcus, Geitlerinema and Pseudanabaena.”
Quote in the paperNot a substantial claim - Findingown data
The majority of branches in the phylogenomic tree are well supported.
“The majority of branches in this phylogeny are well supported.”
Quote in the paperNot a substantial claim - Findingown data
In all analyses, subsections IV and V capable of cellular differentiation have a higher probability of origination close to the minimum age range of the specified prior calibration (1.9-2.1 Ga).
“In all analyses, subsections IV and V capable of cellular differentiation (calibration 2; Fig. 4) have a higher probability of origination close to the minimum age range of our specified prior calibration (1.9–2.1 Ga).”
Quote in the paperNot a substantial claim- The authors state this as an assumption: The most recent common ancestor of subsections IV and V cyanobacteria originated after the GOE but before 1.957 Ga.
- Findingown data
Phylogenomic results confirm previous suggestions of early multicellularity in cyanobacteria.
“Phylogenomic results show increased tree support compared to single‐gene analyses and confirm previous suggestions of early multicellularity in cyanobacteria (Schirrmeister et al. 2013).”
Quote in the paperSubstantial claim - Findingown data
Differentiated cyanobacteria belonging to subsections IV and V are the only groups where morphological and genomic data congruently suggest a monophyletic origin.
“Differentiated cyanobacteria belonging to subsections IV and V are the only groups where morphological and genomic data congruently suggest a monophyletic origin.”
Quote in the paperNot a substantial claim - Findingown data
Phylogenomic results show increased tree support compared to single-gene analyses.
“Phylogenomic results show increased tree support compared to single‐gene analyses and confirm previous suggestions of early multicellularity in cyanobacteria (Schirrmeister et al. 2013).”
Quote in the paperSubstantial claim - Findingown data
If the node for subsections IV and V was not used for calibration, a younger age is estimated (0.8-1.6 Ga).
“However, if this node was not used for calibration, a younger age is estimated (0.8–1.6 Ga; Fig. S4).”
Quote in the paperNot a substantial claim - Findingnone given
Monophyly of cyanobacteria forming heterocysts and akinetes is confirmed in this study.
“Monophyly of cyanobacteria forming heterocysts and akinetes is confirmed in this study.”
Quote in the paperNot a substantial claim - Findingown data
Phylogenomic data fully support monophyly of subsections IV and V cyanobacteria capable of cellular differentiation.
“Phylogenomic data fully support monophyly of subsections IV and V cyanobacteria capable of cellular differentiation.”
Quote in the paperNot a substantial claim - Findingnone given
Clades 1-6 reconstructed in this study can be directly compared to clades A-C, E, F reconstructed by Shih et al. (2013).
“Clades 1–6 (this study) can be directly compared to clades (A–C, E, F) reconstructed by Shih et al. (2013).”
Quote in the paperNot a substantial claim - Findingown data
In one analysis, a younger age (0.8-1.6 Ga) is estimated.
“a younger age is estimated (0.8–1.6 Ga; Fig. S4).”
Quote in the paperNot a substantial claim - Findingown data
Confidence intervals are smaller in general in this study compared with previous analyses based on 16S rRNA data, particularly for deep node ages.
“In comparison with the previous analyses based on 16S rRNA data (Schirrmeister et al. 2013), confidence intervals are smaller in general, particularly those of deep node ages.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Schirrmeister et al. 2013
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- Findingown data
All analyses, irrespective of prior assumptions for node 69, point to an origin of multicellularity in cyanobacteria before the GOE.
“Nevertheless, all analyses, irrespective of the prior assumptions applied for ‘node 69’, point to an origin of multicellularity in cyanobacteria before the GOE (Fig. 5).”
Quote in the paperSubstantial claim - Findingown data
Different widths for the calibration of the root did not affect age estimates for node 69.
“Different widths for the calibration of the root (A, C vs. B, D in Fig. 5) did not affect age estimates for node 69”
Quote in the paperNot a substantial claim - Findingown data
In Hypothesis 1, a calibration of the root between 3.85 and 2.958 resulted in a mean estimate of 235 million years older age for node 69 with wider posterior probability distribution.
“whereas in Hypothesis 1 a calibration of the root between 3.85 and 2.958 resulted in a mean estimate of 235 million years older age for node 69 with wider posterior probability distribution.”
Quote in the paperNot a substantial claim - Findingown data
Posterior node age estimates show large 95% confidence intervals, preventing precise dating of divergence events.
“Posterior node age estimates show large 95% confidence intervals, which prevents a precise dating of divergence events.”
Quote in the paperNot a substantial claim - Findingown data
The majority of modern cyanobacterial clades (clades 2-6) evolved after the GOE.
“The majority of modern cyanobacterial clades (clades 2–6) have evolved after the GOE.”
Quote in the paperSubstantial claim - Findingown data
The results agree with previous estimates of an origin of marine picocyanobacteria around the end of the Mesoproterozoic.
“our results agree with the previous estimates of an origin of marine picocyanobacteria around the end of the Mesoproterozoic (Sanchez‐Baracaldo et al. 2014), although confidence intervals are too broad to specify dates, further.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Sanchez‐Baracaldo et al. 2014
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- Premisenone given
At the end of the Archean Eon, cyanobacteria were responsible for the rapid oxygenation of Earth's atmosphere during the Great Oxidation Event.
“At the end of the Archean Eon, they were responsible for the rapid oxygenation of Earth's atmosphere during an episode referred to as the Great Oxidation Event (GOE).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Bekker et al. 2004
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- cites Anbar et al. 2007
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- Premisecitation
2.0 Ga fossilized resting cells termed Archaeoellipsoides resemble akinetes of modern subsection IV cyanobacterial genus Anabaena.
“Furthermore, 2.0 Ga fossilized resting cells (present in subsections IV and V), termed ‘Archaeoellipsoides’, resemble akinetes of modern subsection IV cyanobacterial genus Anabaena (Amard and Bertrand‐Sarfati 1997).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Amard and Bertrand‐Sarfati 1997
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- Premisecitation
Fossil cyanobacteria from almost all subsections have been found in Mesoproterozoic deposits.
“Fossil cyanobacteria from almost all subsections have been found in Mesoproterozoic deposits (Schopf and Blacic 1971; Horodyski and Donaldson 1980; Butterfield 2000).”
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- cites Horodyski and Donaldson 1980
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- cites Butterfield 2000
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- Premisecitation
In heterotrophic prokaryotes, metabolic rates increase superlinearly with body mass.
“In heterotrophic prokaryotes, metabolic rates have been found to increase superlinearly with body mass (DeLong et al. 2010).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites DeLong et al. 2010
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- Premisecitation
Cyanobacteria belonging to subsections I and III have been identified in the early Proterozoic, including the 1.8 Ga Duck Creek Dolomite and 1.9 Ga Belcher Supergroup.
“Cyanobacteria belonging to subsections I and III have been identified in the early Proterozoic including the 1.8 Ga Duck Creek Dolomite in Australia (Knoll et al. 1988) and 1.9 Ga Belcher Supergroup in Canada (Hofmann 1976).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Knoll et al. 1988
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- cites Hofmann 1976
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- Premisecitation
Attempts to resolve the early evolutionary history of life using molecular phylogenetic approaches have reached contradictory conclusions due to a lack of data and weaknesses in methodology.
“Unfortunately, attempts to resolve the early evolutionary history of life using molecular phylogenetic approaches has reached contradictory conclusions due to a lack of data and weaknesses in methodology (Schirrmeister et al. 2013; Shih and Matzke 2013).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Schirrmeister et al. 2013
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- cites Shih and Matzke 2013
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- Interpretationreasoning
The diversity of cyanobacterial taxa soon after the GOE indicates an origin of cyanobacterial ancestors some time in the Archean.
“The diversity of cyanobacterial taxa soon after the GOE indicates an origin of cyanobacterial ancestors some time in the Archean.”
Quote in the paperSubstantial claim - Premisecitation
Single-gene analyses have limitations, particularly for deep branches.
“However, single‐gene analyses have limitations, particularly for deep branches.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Schirrmeister et al. 2013
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- cites Shih and Matzke 2013
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- Premisecitation
During the early Proterozoic, 2.5-2.3 Ga, atmospheric oxygen levels accumulated rapidly during the Great Oxidation Event as a result of cyanobacterial activity.
“During the early Proterozoic, 2.5–2.3 Ga, atmospheric oxygen levels accumulated rapidly during an episode coined the Great Oxidation Event (GOE; Bekker et al. 2004; Anbar et al. 2007) as a result of cyanobacterial activity leading to great changes to the Earth system (Van Kranendonk et al. 2012), subsequently allowing for the evolutionary emergence of complex life as we know it.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Bekker et al. 2004
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- cites Anbar et al. 2007
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- cites Van Kranendonk et al. 2012
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- Interpretationreasoning
Multicellularity likely had a greater impact on cyanobacterial fitness and thus abundance than previously assumed.
“It is likely that multicellularity had a greater impact on cyanobacterial fitness and thus abundance, than previously assumed.”
Quote in the paperSubstantial claim - Premisenone given
The variety in shapes allows for a fairly reliable identification of cyanobacterial relatives in the fossil record compared to other prokaryotes.
“This variety in shapes allows for a fairly reliable identification of cyanobacterial relatives in the fossil record compared to other prokaryotes.”
Quote in the paperNot a substantial claim - Premisecitation
Programs for molecular clock analyses will truncate prior calibrations so that prior age distributions agree with the occurrences of divergence events in the phylogeny.
“Additionally, Warnock et al. (2012, 2015) pointed out that programs for molecular clock analyses will truncate prior calibrations so that prior age distributions agree with the occurrences of divergence events in the phylogeny.”
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- cites Warnock et al. 2015
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- Premisecitation
The joint (effective) calibration priors may differ substantially from the user-specified priors.
“Therefore, the joint (effective) calibration priors may differ substantially from the user‐specified priors.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Warnock et al. 2012
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- Premisenone given
Filament diameters of these fossils are more probabilistic than deterministic as evidence for the presence of cyanobacteria.
“Filament diameters of these fossils are more probabilistic than deterministic as evidence for the presence of cyanobacteria.”
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Fossil resting cells, akinetes, only present in cyanobacteria capable of heterocyst formation (subsections IV and V), have been described from c. 2.1 Ga Franceville Group, Gabon.
“Fossil resting cells, so called akinetes, only present in cyanobacteria capable of heterocyst formation (subsections IV and V; Fig. 1) have been described from c. 2.1 Ga Franceville Group, Gabon (Amard and Bertrand‐Sarfati 1997; Sergeev 2009).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Amard and Bertrand‐Sarfati 1997
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- cites Sergeev 2009
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- Interpretationreasoning
The majority of modern cyanobacteria are descendants of an ancient multicellular lineage.
“Hence, the majority of modern cyanobacteria are descendants of an ancient multicellular lineage.”
Quote in the paperSubstantial claim - Premisecitation
The upper limit for calibration 1 represents the latest ending of the Late Heavy Bombardment, based on estimates for the end of the strong meteorite bombardment of the moon.
“The upper limit represents the latest ending of the Late Heavy Bombardment, based on estimates for the end of the strong meteorite bombardment of the moon (Stöffler and Ryder 2001; Chapman et al. 2007).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Stöffler and Ryder 2001
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- cites Chapman et al. 2007
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Divergence time results are strongly affected by parameter choice if non-uniform prior calibration densities, such as lognormal, are employed.
“Divergence time results are strongly affected by parameter choice if non‐uniform prior calibration densities, such as lognormal, are employed (Warnock et al. 2012, 2015); therefore, only uniform distributions were applied in this study.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Warnock et al. 2012
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- cites Warnock et al. 2015
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Based on U-Pb zircon ages, rocks containing these Mo signatures were formed at a minimum of 2.940 Ga ± 0.022 Gyr.
“Based on U–Pb zircon ages, rocks containing these Mo signatures were formed at a minimum of 2.940 Ga ± 0.022 Gyr (Hegner et al. 1984).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Hegner et al. 1984
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- Premisecitation
Filamentous fossils from the 3.42-3.35 Ga Strelley Pool Formation, Barberton Greenstone Belt, and possibly earlier evidence the presence of multicellular prokaryotes.
“Filamentous fossils from the 3.42–3.35 Ga found in the Strelley Pool Formation, Australia (Wacey et al. 2011; Sugitani et al. 2013), Barberton Greenstone Belt, South Africa (Walsh 1992; Westall et al. 2001; Westall et al. 2006), and possibly earlier (Awramik et al. 1988; Schopf and Kudryavtsev 2009) evidence the presence of multicellular prokaryotes.”
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Carbon isotope analyses from rocks of similar age, such as Mushandike, Zimbabwe, and Steep Rock, Canada, support an early presence of oxygen as a result of oxygenic photosynthesis.
“Carbon isotope analyses from rocks of similar age, such as Mushandike, Zimbabwe, and Steep Rock, Canada, further support an early presence of oxygen as a result of oxygenic photosynthesis (Nisbet et al. 2007; Nisbet and Nisbet 2008).”
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- cites Nisbet and Nisbet 2008
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Larger tubes (10-20 μm) observed in 3.4 Ga deposits from Western Australia show few characteristics to link them to modern prokaryotic taxa.
“While an occurrence of larger tubes (10–20 μm) has been observed in 3.4 Ga deposits from Western Australia, these show few characteristics to link them to modern prokaryotic taxa.”
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Geochemical evidence based on Mo and Fe isotopes supports an early evolution of oxygenic photosynthesis.
“Geochemical evidence, based on Mo and Fe isotopes, supports an early evolution of oxygenic photosynthesis (Nisbet and Fowler 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Nisbet and Fowler 2011
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- Premisecitation
Modern cyanobacteria exhibit a wide range of cell sizes which, on average, exceeds sizes found among most prokaryotes (<2 μm).
“Modern cyanobacteria exhibit a wide range of cell sizes which, on average, exceeds sizes found among most prokaryotes (<2 μm; Castenholz 2001).”
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Shih and Matzke's results are based on merely two subunits of one enzyme (c. 986 amino acids).
“their results are based on merely two subunits of one enzyme (c. 986 amino acids).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Shih and Matzke (2013)
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- Premisecitation
In c. 2.0 Ga deposits from Western Australia, filaments of large size (63 μm in width) have been found and classified as Oscillatoriopsis majuscule.
“In c. 2.0 Ma deposits from Western Australia, filaments of large size (63 μm in width) have been found and classified as Oscillatoriopsis majuscule (Knoll et al. 1988).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Knoll et al. 1988
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Over time it becomes more likely that sequences saturate, which is a problem particularly for nucleotide sequences and deep branches.
“over time it will become more likely that sequences saturate, which is a problem particularly for nucleotide sequences and deep branches (Xia et al. 2003).”
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The first larger, well-preserved, multicellular morphotypes with cell widths of up to 28 μm can be observed in the 2.6 Ga Transvaal Group.
“The first larger, well‐preserved, multicellular morphotypes with cell widths of up to 28 μm can be observed in the 2.6 Ga Transvaal Group (Altermann and Schopf 1995).”
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- Interpretationreasoning
This has significance for the interpretation of filamentous fossils as cyanobacteria based on their morphology, including those from a range of sites at 2.0 Ga and potentially from the 2.6 Ga Transvaal Supergroup or even older.
“This has some significance for the interpretation of filamentous fossils as cyanobacteria based on their morphology, including those described from a range of sites at 2.0 Ga (Knoll et al. 1988; Lanier 1989; Amard and Bertrand‐Sarfati 1997) and potentially from the 2.6 Ga Transvaal Supergroup (Altermann and Schopf 1995) or even older (Awramik et al. 1988; Schopf and Kudryavtsev 2009).”
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- cites Lanier 1989
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- cites Amard and Bertrand‐Sarfati 1997
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Often, sizes of unicellular taxa exceed those of fossilized filaments, as observed in deposits such as Dismal Lake, Gunflint Chert, Belcher Supergroup and Barberton Supergroup.
“Often, sizes of unicellular taxa exceed those of fossilized filaments, as observed in deposits, such as Dismal Lake, Gunflint Chert, Belcher Supergroup and Barberton Supergroup (Hofmann 1976; Horodyski and Donaldson 1980; Lanier 1989; Walsh 1992).”
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- cites Horodyski and Donaldson 1980
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- cites Lanier 1989
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Fossils of such sizes resemble modern filamentous cyanobacterial sizes observed in the form of genera Lyngbya, Oscillatoria and Trichodesmium.
“Fossils of such sizes resemble modern filamentous cyanobacterial sizes observed in the form of genera Lyngbya, Oscillatoria and Trichodesmium (Castenholz 2001).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Castenholz 2001
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- Premisecitation
These previous results were based on a minimal data set of 16S ribosomal RNA sequences (1077-1090 nucleotide sites).
“However, these results were based on a minimal data set of 16S ribosomal RNA sequences (1077–1090 nucleotide sites).”
Quote in the paperSubstantial claim - Interpretationreasoning
The chances are high that phylogenetic information may have been lost due to multiple substitutions at the same nucleotide site (saturation).
“Therefore, the chances are high that phylogenetic information may have been lost due to multiple substitutions at the same nucleotide site (saturation).”
Quote in the paperSubstantial claim - Interpretationreasoning
Reconstructed phylogenies of an enzyme may result in strongly misleading inferences for species evolution.
“the reconstructed phylogenies depict the evolution of an enzyme and may result in strongly misleading inferences for species evolution.”
Quote in the paperSubstantial claim - Premisecitation
In early Archean deposits, such as in South Africa (3.33-3.46 Ga), fossil filament sizes do not exceed 5 μm.
“In early Archean deposits, such as in South Africa (3.33–3.46 Ga), fossil filament sizes do not exceed 5 μm (Walsh 1992; Westall et al. 2001).”
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- cites Westall et al. 2001
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In modern mat communities, multicellular cyanobacteria such as Oscillatoria and Phormidium move vertically to position themselves in optimal light.
“In modern mat communities, multicellular cyanobacteria, such as Oscillatoria and Phormidium, move vertically to position themselves in optimal light (Stal 1995).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Stal 1995
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- Interpretationreasoning
Potential advantages of multicellularity such as movement and improved substrate attachment in combination with potential increases in metabolic rates could have been the trigger for evolutionary success of cyanobacteria at the end of the Archean initiating the oxygenation of Earth.
“Therefore, potential advantages of multicellularity such as: (1) movement and (2) improved substrate attachment in combination with potential increases in metabolic rates could have been the trigger for evolutionary success of cyanobacteria at the end of the Archean initiating the oxygenation of Earth.”
Quote in the paperNot a substantial claim - Premisecitation
Cellular differentiation in Cyanobacteria can only evolve in a multicellular setting.
“Cellular differentiation in Cyanobacteria, for example, can only evolve in a multicellular setting (Rossetti et al. 2010).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Rossetti et al. 2010
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- Premisecitation
Larger surface area of filamentous bacteria increases contact to the substrate which could have resulted in improved attachment.
“Larger surface area of filamentous bacteria increases contact to the substrate which could have resulted in improved attachment (Young 2006).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Young 2006
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- Interpretationcitation
Multicellularity may have been advantageous during initial substrate attachment at the beginning of mat formation.
“Furthermore, multicellularity may have been advantageous during initial substrate attachment at the beginning of mat formation (Fig. 6).”
Quote in the paperNot a substantial claim - Premisecitation
During cyanobacterial evolution, UV radiation must have been a strong selective pressure resulting in several cyanobacterial taxa today that have developed a capability to protect themselves from UV-A and UV-B using pigments such as scytonemin and shinorine.
“During cyanobacterial evolution, UV radiation must have been a strong selective pressure resulting in several cyanobacterial taxa, today, that have developed a capability to protect themselves from UV‐A and UV‐B using pigments, such as scytonemin and shinorine (Sinha and Häder 2008; Balskus and Walsh 2010; Calteau et al. 2014; Rastogi et al. 2014).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Sinha and Häder 2008
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- cites Balskus and Walsh 2010
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- cites Calteau et al. 2014
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- Interpretationreasoning
Improved attachment of filamentous cyanobacteria at the end of the Archean could have increased mat formation and consequently success of cyanobacterial taxa associated with those microbial communities.
“Improved attachment of filamentous cyanobacteria at the end of the Archean could have increased mat formation and consequently success of cyanobacterial taxa associated with those microbial communities.”
Quote in the paperSubstantial claim - Premisecitation
Prior to the GOE, before an ozone shield was established, additional UV radiation between 200 and 300 nm (UV-C) would have had lethal effects on organisms.
“Prior to the GOE, before an ozone shield was established, additional ultraviolet (UV) radiation between 200 and 300 nm (UV‐C) would have had lethal effects on organisms (Kasting and Catling 2003).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Kasting and Catling 2003
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- Interpretationcitation
The ability to move within the microbial mat, a characteristic described for multicellular cyanobacteria, could have been of great advantage to avoid lethal radiation.
“The ability to move within the microbial mat, a characteristic that has been described for multicellular cyanobacteria, could have been of great advantage to avoid lethal radiation.”
Quote in the paperNot a substantial claim - Premisecitation
Filamentous cyanobacteria of the genus Oscillatoria have been associated with initial substrate colonization during mat formation.
“Filamentous cyanobacteria of the genus Oscillatoria have been associated with initial substrate colonization during mat formation (Stal et al. 1985).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Stal et al. 1985
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- Premisecitation
Fe(II) inhibits growth in Synechococcus cultures.
“It has been shown that Fe (II) inhibits growth in Synechococcus cultures (Swanner et al. 2015).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Swanner et al. 2015
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- Interpretationreasoning
An observed delay in oxygen accumulation until the GOE could have been associated not only with oxygen sinks that remove oxygen, but possibly also with decreased evolutionary success of early Cyanobacteria.
“An observed delay in oxygen accumulation until the GOE could have been associated not only with oxygen sinks that remove oxygen, but possibly also with decreased evolutionary success of early Cyanobacteria.”
Quote in the paperSubstantial claim - Premisecitation
Metabolic rates seem to increase superlinearly with size in heterotrophic bacteria.
“As we have already observed, metabolic rates seem to increase superlinearly with size in heterotrophic bacteria (DeLong et al. 2010).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites DeLong et al. 2010
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- Classified as probably not a substantial claim. 20
- May combine two claims. 34
Probably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataAn evolutionary model assuming equal transition rates resulted in a rate of 0.7575 (standard deviation = 0.1978).
“An evolutionary model assuming equal transition rates resulted in rates of 0.7575 (standard deviation = 0.1978).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataClade 6 comprises the majority of the subsections I to III cyanobacteria and is well supported in the phylogenomic tree, but not resolved in the ribosomal tree.
“‘Clade 6’ comprises the majority of the subsections I to III cyanobacteria (except marine picocyanobacteria, hot spring Synechococcus and early‐branching multicellular taxa) and is well supported in the phylogenomic tree, but not resolved in the ribosomal tree (BS: 41%).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataFor the cyanobacterial stem lineage, posterior age estimates were almost uniformly distributed in Hypothesis 1 and shifted towards an origin of cyanobacteria prior 3.5 Ga for Hypothesis 2.
“For the cyanobacterial stem lineage (calibration 1; Fig. 4), posterior age estimates were almost uniformly distributed in Hypothesis 1 and shifted towards an origin of cyanobacteria prior 3.5 Ga for Hypothesis 2.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataAcross the phylogeny, multicellularity is subsequently lost at least five times and regained on one, possibly two, branch leading to Leptolyngbya sp. PCC 7376 and Spirulina subsalsa PCC 9445.
“Across the phylogeny, multicellularity is subsequently lost at least five times and regained on one, possibly two, branch leading to Leptolyngbya sp. PCC 7376 and Spirulina subsalsa PCC 9445.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown data100% maximum likelihood bootstrap values supported 24 of 64 branches of the ribosomal tree, whereas 100% bootstrap support was inferred for 57 of 64 branches of the genomic tree.
“While 100% maximum likelihood bootstrap (BS) values supported just 24 of 64 branches of the ribosomal tree, 100% bootstrap support was inferred for 57 of 64 branches of the genomic tree.”
Quote in the paperSubstantial claimMay combine two claims.
FindingcitationThe use of a large data set (197,766 amino acid sites) helped overcome limitations of previous analyses, substantially improving statistical support across cyanobacterial phylogeny compared with single-gene analyses, and corroborating hypotheses of an early origin of multicellularity in Cyanobacteria.
“In this study, the use of an impressively large data set (197 766 amino acid sites) helped to overcome the limitations previous analyses might have had, not only substantially improving the statistical support across cyanobacterial phylogeny in comparison with single‐gene analyses, but also corroborating the hypotheses of an early origin of multicellularity in Cyanobacteria (Schirrmeister et al. 2”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Schirrmeister et al. 2011b, 2013
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Findingown dataOur results show that multicellularity evolved very early among cyanobacteria and divergence time estimations confirm previous suggestions of an origin of multicellularity prior to the GOE, independently of whether the 2.0 Ga fossil akinete calibration is used.
“Our results show that multicellularity evolved very early among cyanobacteria and divergence time estimations (Fig. 5) confirm previous suggestions of an origin of multicellularity prior to the GOE, independently of whether the 2.0 Ga fossil akinete calibration is used.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationCyanobacteria exhibit impressive morphological diversity and have been classified into five subsections.
“In addition to their ecological variety, cyanobacteria exhibit impressive morphological diversity, particularly for prokaryotes. On this basis, cyanobacteria have been classified and divided into five subsections (Rippka et al. 1979; Castenholz 2001).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Rippka et al. 1979
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- cites Castenholz 2001
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InterpretationcitationThe transition to multicellularity with its increase in overall size could have had a similar effect on metabolic rates in cyanobacteria.
“The transition to multicellularity with its increase in overall size could have had a similar effect in cyanobacteria.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Premisenone givenCurrent competing hypotheses that attempt to explain the origin of cyanobacteria ignore the possibility of evolutionary innovations that could have influenced fitness and abundance of cyanobacteria.
“These hypotheses, however, ignore the possibility of evolutionary innovations that could have influenced fitness and, hence, abundance of cyanobacteria.”
Quote in the paperSubstantial claimMay combine two claims.
InterpretationreasoningMulticellularity may have served to overcome evolutionary constraints and enabled diversification of the variety of morphotypes seen in cyanobacteria today.
“Multicellularity, as a major evolutionary innovation, forming a novel unit for selection to act upon, may have served to overcome evolutionary constraints and enabled diversification of the variety of morphotypes seen in cyanobacteria today.”
Quote in the paperSubstantial claimMay combine two claims.
PremisereasoningDifficulties in obtaining accurate age estimates for deep speciation events include lack of evolutionary information in molecular data, weaknesses in the phylogenetic model, and paucity of calibration points.
“Difficulties in obtaining accurate age estimates for such deep speciation events may include: (1) the lack of evolutionary information retained in molecular data over such long timescales; (2) weaknesses in the phylogenetic model to correctly infer evolutionary processes that took place over such long time periods; and (3) the paucity of calibration points for divergence time estimation.”
Quote in the paperNot a substantial claimMay combine two claims.
Premisenone givenFurther difficulties of calibrations involve potential misassignment to clades and the likelihood that the age of calibrating fossils is a poor approximation of their clade age.
“Further difficulties of calibrations involve: (1) the potential for their misassignment to clades; and (2) the likelihood that the age of the calibrating fossils is a poor approximation of their clade age.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationAlthough the limiting factor on precision in divergence time studies is uncertainty associated with fossil calibrations, much of the uncertainty associated with phylogeny and divergence time estimation can be diminished by employing genome scale data.
“Although the limiting factor on precision in divergence time studies is invariably the uncertainty associated with the fossil calibrations (dos Reis and Yang 2013), in terms of the degree to which fossil minima approximate the true time of divergence, much of the uncertainty associated with phylogeny and divergence time estimation can be diminished by employing genome scale data (dos Reis et al. 2”
Quote in the paperSubstantial claim0 of 2 sources checked- cites dos Reis and Yang 2013
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- cites dos Reis et al. 2012
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PremisecitationThe overall fossil record is patchy and provides only glimpses into the history of early prokaryotes.
“Although many multicellular fossil remains from the Archean and Proterozoic (Altermann and Schopf 1995; Schopf 2006) have been interpreted as cyanobacteria, the overall fossil record is patchy at best and provides only glimpses into the history of these early prokaryotes.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Altermann and Schopf 1995
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- cites Schopf 2006
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PremisecitationThe appearance of cyanobacterial fossils attributed to subsections IV and V occurs after the GOE, supporting the hypothesis that heterocyst formation evolved after the increase in atmospheric oxygen.
“The appearance of cyanobacterial fossils attributed to subsections IV and V cyanobacteria occurs after the GOE, supporting the hypothesis that heterocyst formation evolved after the increase in atmospheric oxygen to allow for nitrogen fixation, spatially separated from photosynthesis (Tomitani et al. 2006).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Tomitani et al. 2006
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PremisecitationSubsections IV and V cyanobacteria can form differentiated cells such as heterocysts for nitrogen fixation and akinetes.
“bacteria in subsections IV and V have the ability to form differentiated cells, such as metabolically specialized heterocysts for nitrogen fixation and resting cells, so called akinetes (Flores and Herrero 2010).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Flores and Herrero 2010
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PremisecitationSubsection V cyanobacteria are the only cyanobacteria that grow multiseriate filaments and exhibit true branching.
“Taxa belonging to subsection V are the only cyanobacteria that grow multiseriate filaments (varying cell width) and in several planes exhibit ‘true’ branching, not to be confused with ‘false’ branching (Rippka et al. 1979; Gugger and Hoffmann 2004).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Rippka et al. 1979
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- cites Gugger and Hoffmann 2004
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PremisecitationCyanobacteria are among the most ancient evolutionary lineages and may have originated before 3.0 Ga.
“Cyanobacteria are among the most ancient of evolutionary lineages, oxygenic photosynthesizers that may have originated before 3.0 Ga, as evidenced by free oxygen levels.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Crowe et al. 2013
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- cites Lyons et al. 2014
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Study design and conductown dataAge ranges of specified and effective priors were similar and could be accepted for the divergence time analyses.
“Age ranges of specified and effective priors were similar, however, and could be accepted for the divergence time analyses.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown dataFor all analyses, accepted changes to the chains had values of approximately 30% at the time of convergence.
“For all analyses, accepted changes to the chains had values of approximately 30% at the time of convergence.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationBased on Sm-Nd isotopes, two kerogen-rich shale samples of the Franceville Group were dated 2.099 Ga ± 115 Myr to 2.036 Ga ± 79 Myr, suggesting a conservative minimum constraint for tree calibration of 1.957 Ga.
“Based on Sm‐Nd isotopes, two kerogen‐rich shale samples of the Franceville Group were dated 2.099 Ga ± 115 Myr to 2.036 Ga ± 79 Myr, which suggests a conservative minimum constrain for the tree calibration of 1.957 Ga (Bros et al. 1992).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Bros et al. 1992
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PremisecitationFor analyses B and D, the lower limit on the age of crown Cyanobacteria is based on the estimated beginning of the GOE.
“For analyses B and D, the lower limit on the age of crown Cyanobacteria is based on the estimated beginning of the GOE (Bekker et al. 2004).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Bekker et al. 2004
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Classified as probably not a substantial claim.
Study design and conductnone givenAll MCMC runs exhibited evidence of sufficient mixing.
“All MCMC runs exhibited evidence of sufficient mixing.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationFossil akinetes classified as Archaeoellipsoides have been reported from various intervals through the Proterozoic, but the microfossils of the Franceville Group are the earliest of these occurrences.
“These fossil akinetes, classified as Archaeoellipsoides, have been reported from various intervals through the Proterozoic (Horodyski and Donaldson 1980; Golubic et al. 1995; Srivastava 2005); however, the microfossils of the Franceville Group are the earliest of these occurrences.”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Horodyski and Donaldson 1980
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- cites Golubic et al. 1995
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- cites Srivastava 2005
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PremisecitationMo isotope evidence from the Sinqeni Fm., Pongola Supergroup, South Africa, indicates indirectly the presence of manganese oxidation, a process that would require abundant free oxygen.
“The lower limit on the age of crown Cyanobacteria in analyses A and C is based on Mo isotope evidence for oxygen production from the Sinqeni Fm., Pongola Supergroup, South Africa, indicating indirectly the presence of manganese oxidation, a process that would require abundant free oxygen (Planavsky et al. 2014).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Planavsky et al. 2014
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Classified as probably not a substantial claim. May combine two claims.
PremisecitationA previous study by Schirrmeister et al. (2013) estimated divergence times pointing towards an origin of cyanobacteria in the Archean Eon, with multicellularity more likely originating before the GOE.
“Applying 16S rRNA sequence data and a set of different calibration assumptions, a previous study by Schirrmeister et al. (2013) estimated divergence times that pointed towards an origin of cyanobacteria in the Archean Eon, with multicellularity more likely originating before the GOE.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Schirrmeister et al. (2013)
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Probably not a substantial claim: may not pass S1 (asserted), S3 (load-bearing). May combine two claims.
PremisecitationPrevious hypotheses have argued for an origin of Cyanobacteria shortly before the GOE, followed by a rapid accumulation of oxygen as observed during the GOE.
“Previous hypotheses have argued for an origin of Cyanobacteria shortly before the GOE (Kirschvink and Kopp 2008), followed by a rapid accumulation of oxygen as observed during the GOE.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Kirschvink and Kopp 2008
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PremisecitationMore than 2.83-Gyr-old reef systems from Mushandike, Zimbabwe, and Steep Rock, Canada, seem to have been formed in oxic waters and support hypotheses of Archean oxygen oases based on the absence of mass-independent sulphur fractionation.
“More than 2.83‐Gyr‐old reef systems from Mushandike, Zimbabwe, and Steep Rock, Canada, seem to have been formed in oxic waters and support the hypotheses of Archean oxygen oases that were based on the absence of mass‐independent sulphur fractionation (Ohmoto et al. 2006).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Ohmoto et al. 2006
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Premisenone given16S rRNA comprises merely 1400 nucleotide sites with only half of them susceptible to change in phylum Cyanobacteria.
“it comprises merely 1400 nucleotide sites with only half of them susceptible to change in phylum Cyanobacteria.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationCalibrations of tip clades have been claimed to be unsuitable for accurate estimation of deep divergence events.
“Additionally, calibrations of tip clades have been claimed to be unsuitable for the accurate estimation of deep divergence events (Duchene et al. 2014).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Duchene et al. 2014
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PremisecitationSeveral studies have found evidence of free oxygen and inferred the presence of cyanobacteria hundreds of millions of years prior to the GOE, possibly as early as 3.0 Ga.
“Alternatively, several studies have found evidence of free oxygen and, thus, inferred the presence of cyanobacteria, hundreds of millions of years prior to the GOE, possibly as early as 3.0 Ga (Nisbet et al. 2007; Nisbet and Nisbet 2008; Crowe et al. 2013; Lyons et al. 2014).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Nisbet et al. 2007
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- cites Nisbet and Nisbet 2008
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- cites Crowe et al. 2013
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PremisecitationShih and Matzke (2013) recovered a much more recent origin of living cyanobacterial taxa, concluding that an ancient cyanobacterial stem lineage must be responsible for late Archean oxygen levels.
“Another study by Shih and Matzke (2013) recovered a much more recent origin of living cyanobacterial taxa concluding that an ancient cyanobacterial stem lineage must be responsible for late Archean oxygen levels.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Shih and Matzke (2013)
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PremisecitationIsotopes from organic carbon in these rocks point towards cyanobacterial RuBisCO I activity in those deposits and support an origin of cyanobacteria in the Archean.
“Isotopes from organic carbon in these rocks, additionally, point towards cyanobacterial RuBisCO I activity in those deposits and support an origin of cyanobacteria in the Archean (Nisbet et al. 2007; Nisbet and Fowler 2011).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Nisbet et al. 2007
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- cites Nisbet and Fowler 2011
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PremisecitationThe ATPase subunits resulted from an ancient duplication event before the last common ancestor of all living taxa.
“The ATPase subunits resulted from an ancient duplication event, which occurred before the last common ancestor of all living taxa and has therefore been used in the past to reconstruct the Tree of Life (Iwabe et al. 1989).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Iwabe et al. 1989
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InterpretationreasoningThe assumptions that simple filamentous cyanobacterial taxa were present in 2.0-Gyr-old deposits and that cyanobacteria were responsible for the accumulation of oxygen during the Archean indicate an existence of multicellular cyanobacteria before the GOE.
“The assumptions that: (1) simple filamentous cyanobacterial taxa were present in 2.0‐Gyr‐old deposits; and (2) cyanobacteria were responsible for the accumulation of oxygen during the Archean, indicates an existence of multicellular cyanobacteria before the GOE.”
Quote in the paperNot a substantial claim- The authors state this as an assumption: Simple filamentous cyanobacterial taxa were present in 2.0-Gyr-old deposits.
- The authors state this as an assumption: Cyanobacteria were responsible for the accumulation of oxygen during the Archean.
May combine two claims.
Premisenone givenMicrofossils from Proterozoic and Archean deposits comprise multicellular forms, such as septate and non-septate filaments, and unicellular remains, such as spheres and rods.
“Microfossils from Proterozoic and Archean deposits comprise multicellular forms, such as septate and non‐septate filaments, and unicellular remains, such as spheres and rods.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataThe origin of multicellularity was a major transition in the history of cyanobacteria, forming new units subject to selection, and offering the potential to increase cyanobacterial abundance, consequently initiating the GOE.
“We suggest that the origin of multicellularity was a major transition in the history of cyanobacteria, forming new units to be subject to selection, and offering the potential to increase cyanobacterial abundance, consequently initiating the GOE.”
Quote in the paperSubstantial claimMay combine two claims.
PremisecitationExperiments have demonstrated the movement of filamentous cyanobacteria to avoid UV light, where prevention of movement resulted in UV-induced inhibition of photosynthesis.
“Furthermore, experiments have demonstrated the movement of filamentous cyanobacteria to avoid UV light, where prevention of movement resulted in UV‐induced inhibition of photosynthesis (Kruschel and Castenholz 1998).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Kruschel and Castenholz 1998
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InterpretationcitationIn Archean environments, Fe(II) toxicity could have prohibited oxygenic photosynthesis and subsequently allowed for only little oxygen production.
“In Archean environments, Fe (II) toxicity could have prohibited oxygenic photosynthesis and subsequently allowed for only little oxygen production.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe delay in accumulation of free oxygen until the GOE has been explained by a strongly reducing atmosphere where initially produced oxygen was captured by oxygen sinks, such as reduced volcanic gases.
“The delay in the accumulation of free oxygen until the GOE has been explained by a strongly reducing atmosphere where initially produced oxygen was captured by oxygen sinks, such as reduced volcanic gases (Catling and Claire 2005).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Catling and Claire 2005
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Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).
Interpretationnone givenMulticellularity could have provided novel possibilities for cyanobacterial diversification and adaptation to new oxygenated habitats.
“Furthermore, multicellularity could have provided novel possibilities for cyanobacterial diversification and adaptation to new oxygenated habitats.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S4 (based).
InterpretationreasoningAs the only biological source of oxygen during the early Precambrian, cyanobacterial fitness and ecological success should have had a profound impact on the amount of free net oxygen in Earth's ocean and atmosphere.
“As the only biological source of oxygen during the early Precambrian, cyanobacterial fitness and ecological success should have had a profound impact on the amount of free net oxygen in Earth's ocean and atmosphere.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningComparisons of modern cyanobacterial taxa to Precambrian microfossils support the inferred presence of multicellular cyanobacteria before the GOE, but the fossil record does not provide evidence for multicellular taxa among the earliest unequivocal fossil assemblages at 3.33-3.45 Ga.
“Comparisons of modern cyanobacterial taxa to Precambrian microfossils support the inferred presence of multicellular cyanobacteria before the GOE, but the fossil record does not provide evidence for multicellular taxa among the earliest unequivocal fossil assemblages at 3.33–3.45 Ga.”
Quote in the paperSubstantial claimMay combine two claims.
InterpretationreasoningMulticellularity provides selective advantage during early Earth history including movement within microbial mats to avoid lethal UV-C dosages and improved attachment to surfaces during initial mat formation that may have substantially increased the success of cyanobacterial-dominated mat communities and enabled adaptation to novel habitats.
“Multicellularity provides selective advantage during early Earth history including: (1) movement within microbial mats to avoid lethal UV‐C dosages; and (2) improved attachment to surfaces during initial mat formation that may have substantially increased the success of cyanobacterial‐dominated mat communities and enabled adaptation to novel habitats.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S4 (based). May combine two claims.
InterpretationreasoningIncreased sizes of multicellular cyanobacteria may have resulted in higher metabolic rates, hence higher photosynthetic activity and increased net oxygen production.
“Similarly, increased sizes of multicellular cyanobacteria may have resulted in higher metabolic rates, hence, higher photosynthetic activity and increased net oxygen production.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing), S4 (based).
Interpretationnone givenMulticellular growth may have provided competitive advantages that resulted in higher growth success.
“Additionally, multicellular growth may have provided competitive advantages that resulted in a higher growth success (Fig. 6).”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataCyanobacteria originated in the mid-Archean, long before the GOE, with multicellular taxa evolving towards the end of the Archean.
“Cyanobacteria originated in the mid‐Archean, long before the GOE, with multicellular taxa evolving towards the end of the Archean.”
Quote in the paperSubstantial claim
The authors state this as an assumption.
The divergence of the Gloeobacter lineage from the stem lineage leading to all other extant cyanobacteria occurred between 3.85 and 2.918 Ga (analyses A, C) or between 3.85 and 2.45 Ga (analyses B, D).
“The divergence of Gloeobacter lineage from the stem lineage leading to the all other extant cyanobacterial species was assumed to have occurred some time between 3.85 and 2.918 Ga (Table 1, analyses A, C) or 3.85 and 2.45 Ga (Table 1, analyses B, D), with each time point being equally likely (uniform prior distribution).”
The authors state this as an assumption.
The most recent common ancestor of subsections IV and V cyanobacteria originated after the GOE but before 1.957 Ga.
“we assumed that the most recent common ancestor of subsections IV and V cyanobacteria must have originated after the GOE, but prior to 1.957 Ga.”
The authors state this as an assumption.
The end of the Late Heavy Bombardment at 3.85 Ga can be taken as a similar age for Earth.
“Given that the heavy lunar bombardment is estimated to have ended at 3.85 Ga, a similar age may be assumed for Earth given the proximity of the moon.”
The authors state this as an assumption.
Simple filamentous cyanobacterial taxa were present in 2.0-Gyr-old deposits.
“The assumptions that: (1) simple filamentous cyanobacterial taxa were present in 2.0‐Gyr‐old deposits; and (2) cyanobacteria were responsible for the accumulation of oxygen during the Archean, indicates an existence of multicellular cyanobacteria before the GOE.”
The authors state this as an assumption.
Cyanobacteria were responsible for the accumulation of oxygen during the Archean.
“The assumptions that: (1) simple filamentous cyanobacterial taxa were present in 2.0‐Gyr‐old deposits; and (2) cyanobacteria were responsible for the accumulation of oxygen during the Archean, indicates an existence of multicellular cyanobacteria before the GOE.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Cyanobacteria probably evolved during the Archean.
“For example, cyanobacteria probably evolved [e.g., (3)] during this period”
From The Archean atmosphere (2020) · cites this paper as [3]
Most studies suggest an earlier Paleoarchean or Mesoarchean age for oxygenic photosynthesis.
“While some argue that oxygenic photosynthesis evolved only 50 to 100 Ma before the GOE (115), most studies suggest an earlier Paleoarchean or Mesoarchean age [e.g., (3, 118, 119)].”
From The Archean atmosphere (2020) · cites this paper as [3]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Differentiated-clade calibration has two upper bounds
MajorThe methods specify an upper bound of 2.45 Ga for the subsections IV and V calibration, but Table 1 gives 2.32 Ga for that calibration in every analysis.
“We assumed a uniform prior calibration density between 1.957 and 2.45 Ga with 5% prior probability that posterior estimates may lie outside this interval (soft bounds).”
“| A, C | Section IV and V | Uniform (sb) | 1.957 | 2.32 | 1.957 | 2.32 |”
Root-calibration assignments are reversed
MajorThe text assigns the 2.918 Ga lower bound to analyses A and C and the 2.45 Ga bound to B and D. Table 1 assigns them the other way around.
“The divergence of Gloeobacter lineage from the stem lineage leading to the all other extant cyanobacterial species was assumed to have occurred some time between 3.85 and 2.918 Ga (Table 1, analyses A, C) or 3.85 and 2.45 Ga (Table 1, analyses B, D)”
“| A, C | Root | Uniform (hb) | 2.45 | 3.85 | 2.45 | 3.85 |”
Supermatrix length changes in the discussion
MinorThe discussion reports 197,766 amino acid sites, while the methods report 197,761 for the same supermatrix.
“an impressively large data set (197 766 amino acid sites)”
“the resultant 197 761 amino acid‐rich supermatrix”
Five stated multicellular strains are six listed strains
MinorThe sampling description says five multicellular strains were sequenced, but its list names six: one each under items 1, 2, 3 and 5, and two Pseudanabaena strains under item 4.
“and five multicellular strains belonging to the filamentous cyanobacteria without cellular differentiation”
“(1) Geitlerinema sp. PCC 8501; (2) Leptolyngbya sp. PCC 73110; (3) Limnothrix redekei PCC 9416; (4) Pseudanabaena sp. PCC 7704 and PCC 7904; and (5) Symploca sp. PCC 8002)”
Figure captions give a different narrow root bound
MinorThe figure caption gives 2.958 Ga as the lower bound of the narrow root calibration, whereas Table 1 gives 2.918 Ga.
“a narrower root calibration (3.85–2.958 Ga)”
“| B, D | Root | Uniform (hb) | 2.918 | 3.85 | 2.918 | 3.85 |”
q01 is assigned to both opposing transitions
MinorThe results define q01 as both the gain and loss of multicellularity. The methods instead define q01 as the gain and q10 as the transition back to unicellularity.
“where q01 defines the transition to multicellularity and q01 the loss of multicellularity.”
“q01 describes the transition to multicellularity and q10 the transition to unicellularity.”
Western Australian deposit is dated in Ma instead of Ga
MinorThe discussion dates the deposit containing Oscillatoriopsis to approximately 2.0 Ma. The methods describe the Western Australian deposit containing that fossil as approximately 2.0 Ga.
“In c. 2.0 Ma deposits from Western Australia, filaments of large size (63 μm in width) have been found and classified as Oscillatoriopsis majuscule (Knoll et al. 1988).”
“Deposits of similar age from the Duck Creek Dolomite in Western Australia (c. 2.0 Ga) contain several fossils similar to the multicellular cyanobacterial genus Lyngbya, named Oscillatoriopsis (Knoll et al. 1988).”
Figure 2 reverses the hypothesis labels
MinorFigure 2 calls an origin before the GOE Hypothesis 1 and an origin after it Hypothesis 2. The results define Hypothesis 1 as after the GOE and Hypothesis 2 as before it.
“Hypothesis 1: Multicellularity originated in cyanobacteria before the Great Oxidation Event (GOE)”
“an origin of multicellularity after the GOE as an adaptation to newly formed (oxygenated) habitats (Hypothesis 1); or (2) an origin of multicellularity before the GOE”
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On the origin of oxygenic photosynthesis and Cyanobacteria
Sánchez‐Baracaldo, P., & Cardona, T. (2019) · New Phytologist · doi:10.1111/nph.16249 · Cited by 291 · see citing works
“Furthermore, the standard heterodimeric photosystems, a defining 87 trait of crown group Cyanobacteria (Figure 3), evolved towards the late Archean (Blank & 88 Sánchez-Baracaldo, 2010; Schirrmeister et al., 2015) or early Paleoproterozoic (Shih et al., 89 2016).”
BackgroundMethodInfluentialCyanobacteria and biogeochemical cycles through Earth history
Sánchez-Baracaldo, P., Bianchini, G., Wilson, J. D., & Knoll, A. H. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2021.05.008 · Cited by 279 · see citing works
Knoll, A. H., & Nowak, M. A. (2017) · Science Advances · doi:10.1126/sciadv.1603076 · Cited by 277 · see citing works
The multicellular nature of filamentous heterocyst-forming cyanobacteria
Herrero, A., Stavans, J., & Flores, E. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw029 · Cited by 243 · see citing works
Oxidative Stress in Bacteria and the Central Dogma of Molecular Biology
Fasnacht, M., & Polacek, N. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.671037 · Cited by 246 · see citing works
“Interestingly, cyanobacteria, which initially caused the great oxidation event (Schirrmeister et al., 2015), are much more susceptible to H2O2 as compared to eukaryotic aquatic microorganisms (Drábková et al.”
BackgroundCyanobacteria evolution: Insight from the fossil record
Demoulin, C., Lara, Y. J., Cornet, L., François, C., Baurain, D., Wilmotte, A., & Javaux, E. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.05.007 · Cited by 239 · see citing works
Comparative genomics reveals insights into cyanobacterial evolution and habitat adaptation
Chen, M., Teng, W., Zhao, L., Hu, C., Zhou, Y., Han, B., Song, L., & Shu, W.-S. (2020) · The ISME Journal · doi:10.1038/s41396-020-00775-z · Cited by 223 · see citing works
Origin of marine planktonic cyanobacteria
Sánchez‐Baracaldo, P. (2015) · Scientific Reports · doi:10.1038/srep17418 · Cited by 201 · see citing works
Solar energy conversion by photosystem II: principles and structures
Shevela, D., Kern, J. F., Govindjee, G., & Messinger, J. (2023) · Photosynthesis Research · doi:10.1007/s11120-022-00991-y · Cited by 200 · see citing works
The possible evolution and future of CO2-concentrating mechanisms
Raven, J. A., Beardall, J., & Sánchez‐Baracaldo, P. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erx110 · Cited by 186 · see citing works
“…a relaxed Bayesian molecular clock approach, suggest that Gloeobacter could have evolved before the GOE (Blank and Sánchez-Baracaldo, 2010; Sánchez-Baracaldo et al., 2014; SánchezBaracaldo, 2015; Schirrmeister et al., 2015, 2016; see also Dillon and Castenholz, 1999; Olsson-Francis et al., 2010).”
BackgroundInfluentialMarsland, R., Cui, W., Goldford, J. E., Sánchez, Á., Korolev, K. S., & Mehta, P. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006793 · Cited by 141 · see citing works
Cyanobacterial evolution during the Precambrian
Schirrmeister, B. E., Sánchez‐Baracaldo, P., & Wacey, D. (2016) · International Journal of Astrobiology · doi:10.1017/s1473550415000579 · Cited by 158 · see citing works
Self-citationHorizontal gene transfer constrains the timing of methanogen evolution
Wolfe, J. M., & Fournier, G. P. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0513-7 · Cited by 160 · see citing works
The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages
Fournier, G. P., Moore, K. R., Rangel, L. T., Payette, J. G., Momper, L., & Bosak, T. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.0675 · Cited by 156 · see citing works
Early Archean origin of Photosystem <scp>II</scp>
Cardona, T., Sánchez‐Baracaldo, P., Rutherford, A. W., & Larkum, A. W. (2019) · Geobiology · doi:10.1111/gbi.12322 · Cited by 144 · see citing works
The pyrenoid: the eukaryotic CO2-concentrating organelle
He, S., Crans, V. L., & Jonikas, M. C. (2023) · The Plant Cell · doi:10.1093/plcell/koad157 · Cited by 115 · see citing works
Evolutionary Patterns of Thylakoid Architecture in Cyanobacteria
Mareš, J., Strunecký, O., Bučinská, L., & Wiedermannová, J. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00277 · Cited by 116 · see citing works
A Metagenomic Approach to Cyanobacterial Genomics
Alvarenga, D. O., Fiore, M. F., & Varani, A. M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00809 · Cited by 110 · see citing works
“Cyanobacteria were amongst the earliest organisms on the planet and synthesized important molecules for primitive life (Banack et al., 2012; Schirrmeister et al., 2016).”
BackgroundMergelov, N. S., Mueller, C. W., Prater, I., Shorkunov, I. G., Dolgikh, A. V., Zazovskaya, E. P., Шишков, В. А., Krupskaya, V. V., Абросимов, К. Н., Cherkinsky, A. E., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-21682-6 · Cited by 110 · see citing works
Arman, T., & Clarke, J. (2021) · Toxins · doi:10.3390/toxins13080537 · Cited by 112 · see citing works
“acids: [1] D-Alanine (D-Ala); [2] Variable L-amino acid (X); [3] D-Methyl aspartic acid (D-MeAsp);”
Evolution of increased complexity and specificity at the dawn of form I Rubiscos
Schulz, L., Guo, Z., Zarzycki, J., Steinchen, W., Schuller, J. M., Heimerl, T., Prinz, S., Mueller‐Cajar, O., Erb, T. J., & Hochberg, G. K. A. (2022) · Science · doi:10.1126/science.abq1416 · Cited by 99 · see citing works
Chen, S., Sun, G., Rosen, B. P., Zhang, S., Deng, Y., Zhu, B., Rensing, C., & Zhu, Y. (2017) · Scientific Reports · doi:10.1038/s41598-017-08313-2 · Cited by 93 · see citing works
Genetic responses to carbon and nitrogen availability in Anabaena
Herrero, A., & Flores, E. (2018) · Environmental Microbiology · doi:10.1111/1462-2920.14370 · Cited by 93 · see citing works
Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA)
Sánchez‐Baracaldo, P., Bianchini, G., Cesare, A. D., Callieri, C., & Chrismas, N. A. M. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00045 · Cited by 81 · see citing works
“Our age estimates for the Syn/Pro clade ∼599 Mya (Figure 1 and Table 1) are consistent with recent studies implementing a Bayesian approach showing their ancestors appearing toward the end of the PreCambrian (Sánchez-Baracaldo et al., 2014; Sánchez-Baracaldo, 2015; Schirrmeister et al., 2015b).”
BackgroundDating phototrophic microbial lineages with reticulate gene histories
Magnabosco, C., Moore, K. R., Wolfe, J. M., & Fournier, G. P. (2018) · Geobiology · doi:10.1111/gbi.12273 · Cited by 83 · see citing works
“Although several molecular clocks have been generated for Cyanobacteria (Dvořák et al., 2014; Falcón et al., 2010; SánchezBaracaldo, 2015; Schirrmeister et al., 2013, 2015; Shih et al., 2017), large differences in outgroup, root prior, and internal calibration selection in these models have…”
BackgroundMethodAn Expanded Ribosomal Phylogeny of Cyanobacteria Supports a Deep Placement of Plastids
Moore, K. R., Magnabosco, C., Momper, L., Gold, D. A., Bosak, T., & Fournier, G. P. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01612 · Cited by 71 · see citing works
“The topologies for the major cyanobacterial groups produced by these different analyses are in general agreement (e.g., Shih et al., 2013; Schirrmeister et al., 2015).”
BackgroundCyanoseq : A database of cyanobacterial 16S rRNA gene sequences with curated taxonomy
Lefler, F. W., Berthold, D. E., & Laughinghouse, H. D. (2023) · Journal of Phycology · doi:10.1111/jpy.13335 · Cited by 68 · see citing works
“…evolved ~ 3.8 Ga ago (Whitton & Potts, 2012), and their ability to perform oxygenic photosynthesis led to the Great Oxygenation Event ~ 2.4– 2 Ga ago, drastically altering the Earth's atmosphere from an oxygen poor to an oxygen rich atmosphere (Lyons et al., 2014; Schirrmeister et al., 2015).”
BackgroundInfluentialXiao, S., & Tang, Q. (2018) · Emerging Topics in Life Sciences · doi:10.1042/etls20170165 · Cited by 64 · see citing works
“…fossil record of akinetes is important, not only because akinete fossils serve key calibrations for molecular clock estimates of the Nostacales [18,59,60], but also because the development of heterocysts has been hypothesized to be an evolutionary innovation in response to rising pO 2 levels…”
BackgroundMantle data imply a decline of oxidizable volcanic gases could have triggered the Great Oxidation
Kadoya, S., Catling, D. C., Nicklas, R. W., Puchtel, I. S., & Anbar, A. D. (2020) · Nature Communications · doi:10.1038/s41467-020-16493-1 · Cited by 72 · see citing works
Lammer, H., Sproß, L., Grenfell, J. L., Scherf, M., Fossati, L., Lendl, M., & Cubillos, P. E. (2019) · Astrobiology · doi:10.1089/ast.2018.1914 · Cited by 67 · see citing works
“However, for bacteria that are suited to a reducing environment, this implies an existential crisis requiring adaption for survival (e.g., Schopf, 2014; Schirrmeister et al., 2015).”
Taxonomic Novelty and Distinctive Genomic Features of Hot Spring Cyanobacteria
Alcorta, J., Alarcón-Schumacher, T., Salgado, O., & Dı́ez, B. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.568223 · Cited by 64 · see citing works
Emerging Species and Genome Editing Tools: Future Prospects in Cyanobacterial Synthetic Biology
Gale, G. A. R., Schiavon Osorio, A. A., Mills, L. A., Wang, B., Lea-Smith, D. J., & McCormick, A. J. (2019) · Microorganisms · doi:10.3390/microorganisms7100409 · Cited by 61 · see citing works
“5 billion years ago in the predecessors to modern-day cyanobacteria [5].”
BackgroundHamilton, T. (2019) · Free Radical Biology & Medicine · doi:10.1016/j.freeradbiomed.2019.05.003 · Cited by 56 · see citing works
Nitrogen-Fixing Heterocystous Cyanobacteria in the Tonian Period
Pang, K., Tang, Q., Chen, L., Wan, B., Niu, C., Yuan, X., & Xiao, S. (2018) · Current Biology · doi:10.1016/j.cub.2018.01.008 · Cited by 56 · see citing works
Luimstra, V. M., Schuurmans, J. M., de Carvalho, C. F. M., Matthijs, H. C. P., Hellingwerf, K. J., & Huisman, J. (2019) · Photosynthesis Research · doi:10.1007/s11120-019-00630-z · Cited by 57 · see citing works
Bishé, B., Taton, A., & Golden, J. W. (2019) · iScience · doi:10.1016/j.isci.2019.09.002 · Cited by 55 · see citing works
Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria
Li, M., Calteau, A., Semchonok, D. A., et al. (2019) · Nature Plants · doi:10.1038/s41477-019-0566-x · Cited by 54 · see citing works
“Genomic context of psaL/I/F/J genes and PsaL protein sequences were extracted from the MicroScope platform (Vallenet et al., 2017), public databases, and data generated in previous study (Schirrmeister et al., 2015) or this study (Dataset S1).”
MethodSelf-citationNitrogenase Inhibition Limited Oxygenation of Earth’s Proterozoic Atmosphere
Allen, J. F., Thake, B., & Martin, W. F. (2019) · Trends in Plant Science · doi:10.1016/j.tplants.2019.07.007 · Cited by 50 · see citing works
The origin and evolution of cyanobacteria
Shestakov, S. V., & Karbysheva, E. A. (2017) · Biology Bulletin Reviews · doi:10.1134/s2079086417040090 · Cited by 51 · see citing works
“in the scale of geological eons based on phylogenomic, geochemical, and paleontological data and the use of modern modeling methods (Nisbet and Fowler, 2011; Larsson et al., 2011; Lyons et al., 2014; Sanchez-Baracaldo et al., 2014; Schirrmeister et al., 2015).”
BackgroundRigonato, J., Gama, W. A., Alvarenga, D. O., Branco, L. H. Z., Brandini, F. P., Genuário, D. B., & Fiore, M. F. (2016) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijsem.0.001066 · Cited by 44 · see citing works
“11 On: Tue, 04 Dec 2018 05:48:57 of these organisms (S anchez-Baracaldo et al., 2005; Blank & S anchez-Baracaldo, 2010; Larsson et al., 2011; Shih et al., 2013; Bombar et al., 2014; Kom arek et al., 2014; Calteau et al., 2014; Chrismas et al., 2015; Schirrmeister et al., 2015).”
BackgroundInfluentialSwanner, E. D., Wu, W., Hao, L., Wuestner, M. L., Obst, M., Moran, D. M., McIlvin, M. R., Saito, M. A., & Kappler, A. A. (2015) · Frontiers in Earth Science · doi:10.3389/feart.2015.00060 · Cited by 44 · see citing works
“As as a coastal representative of Synechococcus , it does not cluster near the base the phylogenetic tree of cyanobacteria (Schirrmeister et al., 2015).”
Cyanobacterial ultrastructure in light of genomic sequence data
Gonzalez-Esquer, C. R., Šmarda, J., Rippka, R., et al. (2016) · Photosynthesis Research · doi:10.1007/s11120-016-0286-2 · Cited by 43 · see citing works
Self-citationOxidoreductases and metal cofactors in the functioning of the earth
Mele, B. H., Monticelli, M., Leone, S., Bastoni, D., Barosa, B., Cascone, M., Migliaccio, F., Montemagno, F., Ricciardelli, A., Tonietti, L., et al. (2023) · Essays in Biochemistry · doi:10.1042/ebc20230012 · Cited by 42 · see citing works
“The great availability of oxygen in earth’s extant atmosphere results from the emergence of oxygenic photosynthesis, which, coupled with a complex series of geological feedbacks, was responsible for the Great Oxidation Event (GOE, 2.5–2.3 billion years ago) [28,29].”
InfluentialToxic effects of cyanotoxins in teleost fish: A comprehensive review
Banerjee, S., Maity, S., Guchhait, R., Chatterjee, A., Biswas, C., Adhikari, M., & Pramanick, K. (2021) · Aquatic Toxicology · doi:10.1016/j.aquatox.2021.105971 · Cited by 44 · see citing works
Zhao, L., Lin, L., Chen, M., et al. (2022) · Water Research · doi:10.1016/j.watres.2022.118385 · Cited by 43 · see citing works
Elainella gen. nov.: a new tropical cyanobacterium characterized using a complex genomic approach
Jahodářová, E., Dvořák, P., Hašler, P., Holušová, K., & Poulíčková, A. (2017) · European Journal of Phycology · doi:10.1080/09670262.2017.1362591 · Cited by 41 · see citing works
Microfossils from the lower Mesoproterozoic Kaltasy Formation, East European Platform
Sergeev, V. N., Knoll, A. H., Vorob’eva, N. G., & Sergeeva, N. D. (2016) · Precambrian Research · doi:10.1016/j.precamres.2016.03.015 · Cited by 41 · see citing works
“within the cyanobacteria and was lost several times (Schirrmeister et al., 2015) or evolved multiple times convergently (Ishida et al.”
BackgroundInfluentialElhai, J., & Khudyakov, I. (2018) · Molecular Microbiology · doi:10.1111/mmi.14003 · Cited by 38 · see citing works
“It is also concordant with three other trees based on different sets of concatenated protein alignments (SánchezBaracaldo et al., 2014; Shih et al., 2014; Schirrmeister et al., 2015).”
BackgroundResultŚlesak, I., Kula-Maximenko, M., Ślesak, H., Miszalski, Z., & Strzałka, K. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.03.004 · Cited by 38 · see citing works
Churro, C., Semedo-Aguiar, A. P., Silva, A., Pereira‐Leal, J. B., & Leite, R. B. (2020) · Scientific Reports · doi:10.1038/s41598-020-64774-y · Cited by 42 · see citing works
Stadnichuk, I. N., & Kusnetsov, V. V. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032290 · Cited by 35 · see citing works
Electron transfer in biological systems
Marques, H. M. (2024) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-024-02076-8 · Cited by 40 · see citing works
Cyanotoxins, biosynthetic gene clusters, and factors modulating cyanotoxin biosynthesis
Bashir, F., Bashir, A., Bouaı̈cha, N., Chen, L., Codd, G. A., Neilan, B. A., Xu, W., Ziko, L., Rajput, V. D., Minkina, T., et al. (2023) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-023-03652-x · Cited by 39 · see citing works
Cyanobacteria in Terrestrial Symbiotic Systems
Rikkinen, J. K. (2017) · Springer eBooks · doi:10.1007/978-3-319-46261-5_8 · Cited by 38 · see citing works
Gloeobacter and the implications of a freshwater origin of Cyanobacteria
Raven, J. A., & Sánchez‐Baracaldo, P. (2021) · Phycologia · doi:10.1080/00318884.2021.1881729 · Cited by 35 · see citing works
“Gleobacter (Schirrmeister et al. 2015) and major clades and taxa (Sánchez-Baracaldo 2015; Sánchez-Baracaldo et al.”
BackgroundCorrales‐Guerrero, L., Camargo, S., Valladares, A., Picossi, S., Luque, I., de Alda, J. A. G. O., & Antonia Herrero, B. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02260 · Cited by 34 · see citing works
“Besides their significant contribution to the primary productivity in the modern oceans, the evolutionary relevance of cyanobacteria is maximum as the organisms that developed oxygenic photosynthesis leading to the Proterozoic oxidation of the Earth’s atmosphere (Schirrmeister et al., 2015) and as the ancestors, via e…”
BackgroundZhang, X., Ye, X., Lv, C., et al. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.136314 · Cited by 31 · see citing works
Oldest thylakoids in fossil cells directly evidence oxygenic photosynthesis
Demoulin, C., Lara, Y. J., Lambion, A., & Javaux, E. (2024) · Nature · doi:10.1038/s41586-023-06896-7 · Cited by 32 · see citing works
“However, the appearance of oxygenic photosynthesis does not need to coincide with the origin of crown cyanobacteria, which diversified before 17,18 or after 19 the GOE.”
Moczydłowska, M., Pease, V., Willman, S., Wickström, L., & Agić, H. (2017) · Geological Magazine · doi:10.1017/s0016756817000085 · Cited by 30 · see citing works
Kamennaya, N. A., Zemla, M., Mahoney, L. E., Chen, L., Holman, E. A., Holman, H. N., Auer, M., Ajo-Franklin, C. M., & Jansson, C. (2018) · Nature Communications · doi:10.1038/s41467-018-04588-9 · Cited by 31 · see citing works
Thapliyal, G., Bhandari, M. S., Vemanna, R. S., Pandey, S., Meena, R. K., & Barthwal, S. (2022) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2022.2092714 · Cited by 29 · see citing works
“This entire cycle is known as the “Great Oxidation Event” (GOE) [139], where the cyanobacteria turned into a significant photosynthetic apparatus and an endosymbiotic organelle (chloroplast) during its evolution.”
BackgroundRiley, K. W., Gonzalez, A., & Risser, D. D. (2018) · Molecular Microbiology · doi:10.1111/mmi.14061 · Cited by 27 · see citing works
“If this is the case, multicellularity may have provided selective advantages during the Earth’s early history that allowed for rapid expansion and diversification of cyanobacteria and led to the resulting rapid increase in atmospheric oxygen levels (Schirrmeister et al., 2015).”
BackgroundInfluentialChenebault, C., Díaz‐Santos, E., Kammerscheit, X., Görgen, S., Ilioaia, C., Streckaitė, S., Gall, A., Robert, B., Marcon, E., Buisson, D., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.586601 · Cited by 28 · see citing works
“Cyanobacteria, the oldest and largest phylum of prokaryotes that perform the plant-like photosynthesis (Schirrmeister et al., 2015), are regarded as the ancestors of the plant chloroplast (Ponce-Toledo et al.”
BackgroundHarada, M., Akiyama, A., Furukawa, R., Yokobori, S., Tajika, E., & Yamagishi, A. (2021) · Journal of Molecular Evolution · doi:10.1007/s00239-021-10021-5 · Cited by 29 · see citing works
Nitrogen depletion in Arthrospira sp. PCC 8005, an ultrastructural point of view
Deschoenmaeker, F., Facchini, R., Cabrera, J. C., Bayon-Vicente, G., Sachdeva, N., Flammang, P., & Wattiez, R. (2016) · Journal of Structural Biology · doi:10.1016/j.jsb.2016.08.007 · Cited by 27 · see citing works
“The metabolic abilities of cyanobacteria also make them useful for industrial applications (e.g. production of biodiesel), and therefore, they have been extensively characterized (Garcia-Pichel, 2009; Schirrmeister et al., 2015).”
BackgroundThe Emergence of Life as a First-Order Phase Transition
Mathis, C., Tanmoy Bhattacharya, A., & Walker, S. I. (2017) · Astrobiology · doi:10.1089/ast.2016.1481 · Cited by 27 · see citing works
“A prominent example is the dramatic change in Earth’s atmosphere due to the evolution of oxygenic photosynthesis (Schirrmeister et al., 2015).”
Schad, M., Konhauser, K. O., Sánchez‐Baracaldo, P., Kappler, A. A., & Bryce, C. C. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.07.014 · Cited by 27 · see citing works
“The question of how oxygenic photosynthesis impacted the Archean (4.0–2.5 Ga) iron cycle should have a rather straightforward answer because the reaction of reduced (ferrous) iron with oxygen is rapid at circumneutral pH.”
BackgroundInfluentialSpatial structure: shaping the ecology and evolution of microbial communities
Bäcker, M., Doekes, H. M., Garza, D. R., Meijer, J., van Vliet, S., Allen, R. J., Hogeweg, P., Dutilh, B. E., & van Dijk, B. (2026) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuaf067 · Cited by 30 · see citing works
“For microbes, broad interpretations include the cyanobacteria-driven, planetary oxygenation of the early Earth (Schirrmeister et al. 2015 ), whereas the secretion of biosurfactants that modify surface properties to enable swarming on surfaces exemplifies the narrow definition of niche construction (Kearns and Losick 2…”
InfluentialHerrmann, A. J., & Gehringer, M. M. (2019) · Geobiology · doi:10.1111/gbi.12339 · Cited by 21 · see citing works
Prebiotic Pathway from Ribose to RNA Formation
Bánfalvi, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22083857 · Cited by 25 · see citing works
Lévesque, J.-P., SUMMERS, K. M., Bisht, K., Millard, S. M., Winkler, I. G., & Pettit, A. R. (2021) · Experimental Hematology · doi:10.1016/j.exphem.2021.08.011 · Cited by 25 · see citing works
Dvořák, P., Hašler, P., Casamatta, D. A., & Poulíčková, A. (2021) · Fottea · doi:10.5507/fot.2021.009 · Cited by 24 · see citing works
“To avoid the problems associated with single–gene phylogenies, multilocus and phylogenomics datasets are also being utilized (Ahlgren et al. 2012; Mazard et al. 2012; Komárek et al. 2014; Schirrmeister et al. 2015; Alvarenga et al. 2017; Mareš 2018).”
BackgroundMethodInfluentialExposure of cyanobacterium Nostoc sp. to the Mars-like stratosphere environment
Ye, T., Wang, B., Li, C., Bian, P., Chen, L., & Wang, G. (2021) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2021.112307 · Cited by 21 · see citing works
Structure and assembly pattern of a freshwater short-tailed cyanophage Pam1
Zhang, J., Yang, F., Du, K., et al. (2021) · Structure · doi:10.1016/j.str.2021.10.004 · Cited by 24 · see citing works
A primordial Orange Carotenoid Protein: Structure, photoswitching activity and evolutionary aspects
Slonimskiy, Y. B., Zupnik, A. O., Varfolomeeva, L. A., et al. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.09.131 · Cited by 21 · see citing works
Sultana, S., Awal, S., Shaika, N. A., et al. (2022) · Aquaculture Research · doi:10.1111/are.16011 · Cited by 23 · see citing works
Cyanobacteria From Brazilian Extreme Environments
Genuário, D. B., Vaz, M. G. M. V., Santos, S. N., Kavamura, V. N., & de Melo, I. S. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814849-5.00016-2 · Cited by 24 · see citing works
Biological Weathering in the Terrestrial System
Zaharescu, D. G., Burghelea, C. I., Dontsova, K. M., Reinhard, C. T., Chorover, J., & Lybrand, R. A. (2020) · Geophysical monograph · doi:10.1002/9781119413332.ch1 · Cited by 26 · see citing works
Ancestral Sequence Reconstructions of MotB Are Proton-Motile and Require MotA for Motility
Islam, M. I., Lin, A., Lai, Y.-W., et al. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.625837 · Cited by 13 · see citing works
“The reliable answer to this question is still not clear as it is not known whether the original swimmer was sodium or proton powered (Schirrmeister et al., 2015).”
BackgroundBianchini, G., Hagemann, M., & Sánchez‐Baracaldo, P. (2024) · Systematic Biology · doi:10.1093/sysbio/syae025 · Cited by 20 · see citing works
“Gloeobacter strains ( G. violaceus PCC 7421 and G. kilaueensis JS1) form a monophyletic sister group to the other cyanobacteria (Seo and Yokota 2003; Hoffmann et al. 2005; Sánchez-Baracaldo et al. 2005; Blank and Sánchez-Baracaldo 2010; Schirrmeister et al. 2015).”
BackgroundAncient balancing selection on heterocyst function in a cosmopolitan cyanobacterium
Sano, E. B., Wall, C. A., Hutchins, P. R., & Miller, S. R. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0435-9 · Cited by 21 · see citing works
Duval, C., Thomazeau, S., Drelin, Y., et al. (2018) · Harmful Algae · doi:10.1016/j.hal.2018.01.008 · Cited by 22 · see citing works
Ribose Selected as Precursor to Life
Bánfalvi, G. (2019) · DNA and Cell Biology · doi:10.1089/dna.2019.4943 · Cited by 20 · see citing works
“Oxygenic photosynthesizer cyanobacteria may have originated before 3 billion years (Schirrmeister et al. , 2015).”
Lamparter, T., Babian, J., Fröhlich, K., Mielke, M., Weber, N. F., Wunsch, N., Zais, F., Schulz, K., Aschmann, V., Spohrer, N., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0249509 · Cited by 21 · see citing works
A theoretical approach to the size-complexity rule
Amado, A., Batista, C., & Campos, P. R. A. (2017) · Evolution · doi:10.1111/evo.13392 · Cited by 19 · see citing works
Role of stellar physics in regulating the critical steps for life
Lingam, M., & Loeb, A. (2019) · International Journal of Astrobiology · doi:10.1017/s1473550419000016 · Cited by 25 · see citing works
“…photosynthesis evolved approximately 2.7 Ga or later (Eigenbrode and Freeman 2006; Falcón et al. 2010; Farquhar et al. 2011; Stüeken et al. 2012; Planavsky et al. 2014; Schirrmeister et al. 2015, 2016; Shih et al. 2017), i.e. a few 100 Myr prior to the onset of the Great Oxygenation Event (GOE).”
BackgroundInfluentialEvolution of cellular metabolism and the rise of a globally productive biosphere
Braakman, R. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.05.004 · Cited by 18 · see citing works
The origin and impeded dissemination of the DNA phosphorothioation system in prokaryotes
Jian, H., Xu, G., Yi, Y., Hao, Y., Wang, Y., Xiong, L., Wang, S., Liu, S., Meng, C., Wang, J., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26636-7 · Cited by 20 · see citing works
Demographic analysis of cyanobacteria based on the mutation rates estimated from an ancient ice core
Segawa, T., Takeuchi, N., Fujita, K., et al. (2018) · Heredity · doi:10.1038/s41437-017-0040-3 · Cited by 20 · see citing works
“Timescale of Cyanobacteria demography and phylogeography Cyanobacteria are the only organisms that have evolved oxygenic photosynthesis, and are some of the most important life forms that influenced Earth environments in the Precambrian (Lane, 2005; Schirrmeister et al. 2015).”
BackgroundEvolution of kaiA, a key circadian gene of cyanobacteria
Dvornyk, V., & Mei, Q. (2021) · Scientific Reports · doi:10.1038/s41598-021-89345-7 · Cited by 20 · see citing works
Mechanisms and climatic-ecological effects of the Great Oxidation Event in the early Proterozoic
Luo, G., Zhu, X., Wang, S., Zhang, S., & Jiao, C. (2022) · Science China Earth Sciences · doi:10.1007/s11430-021-9934-y · Cited by 20 · see citing works
“Multicellular cyanobacteria might have had higher metabolic efficiency, higher ability to adapt to diverse habitats, and higher burial efficiency, which would promote O2 production and thus contribute to the occurrence of the GOE (Schirrmeister et al., 2015).”
BackgroundCyanobacteria in Nitrogen-Fixing Symbioses
Bustos‐Díaz, E. D., Barona‐Gómez, F., & Cibrián‐Jaramillo, A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814667-5.00002-7 · Cited by 19 · see citing works
Diurnal Fe(II)/Fe(III) cycling and enhanced O2 production in a simulated Archean marine oxygen oasis
Herrmann, A. J., Sorwat, J., Byrne, J. M., Frankenberg‐Dinkel, N., & Gehringer, M. M. (2021) · Nature Communications · doi:10.1038/s41467-021-22258-1 · Cited by 18 · see citing works
The Thermosynechococcus Genus: Wide Environmental Distribution, but a Highly Conserved Genomic Core
Prondzinsky, P., Berkemer, S. J., Ward, L. M., & McGlynn, S. E. (2021) · Microbes and Environments · doi:10.1264/jsme2.me20138 · Cited by 17 · see citing works
“…marine environments (Sánchez-Baracaldo, 2015), iii) the transition from unicellular to multicellular organisms for increased evolutionary success (Schirrmeister et al., 2015), iv) the inhibition of early cyanobacteria due to high iron concentrations (Swanner, Mloszewska, et al., 2015; Swanner,…”
BackgroundShimada, Y., Suzuki, T., Matsubara, T., Kitajima‐Ihara, T., Nagao, R., Dohmae, N., & Noguchi, T. (2022) · Nature Communications · doi:10.1038/s41467-022-31931-y · Cited by 19 · see citing works
Ligrone, R. (2019) · Springer eBooks · doi:10.1007/978-3-030-16057-9_5 · Cited by 19 · see citing works
Iron homeostasis of cyanobacteria: advancements in siderophores and metal transporters
Fresenborg, L., Graf, J., Schätzle, H., & Schleiff, E. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-819311-2.00007-3 · Cited by 19 · see citing works
- Authors
- Schirrmeister, B. E., Gugger, M., & Donoghue, P. C. J.
- Affiliations
- University of Bristol (GB)
- Institut Pasteur (FR)
- Venue
- Palaeontology
- Publisher
- Wiley
- Published
- 2015-06-23
- Volume
- 58
- Issue
- 5
- Pages
- 769-785
- ISSN
- 0031-0239 (ISSN-L)
- 1475-4983
- PMC
- PMC4755140
- OpenAlex
- W1831957949
- Semantic Scholar
- 6e03cd37924a78a193bde6f1580e42699eee46c3
- Cited by
- 304
- References
- 102
- Citations by year
- 2026: 24 · 2025: 29 · 2024: 54 · 2023: 31 · 2022: 30 · 2021: 25 · 2020: 21 · 2019: 32 · 2018: 28 · 2017: 18 · 2016: 8 · 2015: 4
- FWCI
- 8.40
- Type
- journal article
- Language
- en
- Update notices
- correction (2015-08-14)
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Palaeontology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Explore Bristol Research (publishedVersion, cc-by)
- HAL (submittedVersion, cc-by)
- Bristol Research (University of Bristol) (submittedVersion, cc-by)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/J00538X/1)
- European Commission (FP7 - PEOPLE - 2012 - IEF) (PIEF-GA-2012-330849)
- Swiss National Science Foundation (PBZHP3_147232)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Keywords
- cyanobacteria, Great Oxidation Event, multicellularity, cyanobacterial evolution, Archean, phylogenomics, character reconstruction, cyanobacterial genome, cyanobacterial diversity
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