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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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A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Relaxed clock analyses provide firm support for an origin of cyanobacteria in the Archean and a transition to multicellularity before the GOE.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- 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).
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Relaxed clock analyses provide firm support for an origin of cyanobacteria in the Archean and a transition to multicellularity before the GOE.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes- 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.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Results of all analyses suggest a very early transition to multicellularity at ‘node/branch 69’ (Fig. 3; Fig. S3; Table S3).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Ancestral character state reconstruction
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In the paper
“Changing the widths of the uniform distribution in several runs supported an early transition to multicellularity even further (Fig. S3, online Supporting Information).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Ancestral character state reconstruction
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesThe paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“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”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Comparison of phylogenetic reconstructions based on genome and ribosomal data
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Divergence time estimation
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesA result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Ancestral character state reconstruction
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In the paper
“Six distinct clades could be reconstructed with full support.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Material and methods > Phylogenomic analyses using a supermatrix
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Divergence time estimation
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In the paper
“The posterior age estimates for the origin of multicellularity (calibration 3) are in all cases shifted towards the older bound of the effective priors.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Divergence time estimation
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- Probably not a substantial claim. 20
- It may state two separate claims as one. 34
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“An evolutionary model assuming equal transition rates resulted in rates of 0.7575 (standard deviation = 0.1978).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Ancestral character state reconstruction
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
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In the paper
“‘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%).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Comparison of phylogenetic reconstructions based on genome and ribosomal data
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Divergence time estimation
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Ancestral character state reconstruction
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Comparison of phylogenetic reconstructions based on genome and ribosomal data
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In the paper
“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”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Improved data set to reconstruct the evolutionary history of Cyanobacteria
What the sources say
- Not checked yetcites Schirrmeister et al. 2011b, 2013
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Comparison of cyanobacterial cell sizes to Precambrian microfossils
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
What the sources say
- Not checked yetcites Rippka et al. 1979
- Not checked yetcites Castenholz 2001
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In the paper
“The transition to multicellularity with its increase in overall size could have had a similar effect in cyanobacteria.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“These hypotheses, however, ignore the possibility of evolutionary innovations that could have influenced fitness and, hence, abundance of cyanobacteria.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
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A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
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The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
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In the paper
“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”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
What the sources say
- Not checked yetcites dos Reis and Yang 2013
- Not checked yetcites dos Reis et al. 2012
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
What the sources say
- Not checked yetcites Altermann and Schopf 1995
- Not checked yetcites Schopf 2006
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
What the sources say
- Not checked yetcites Tomitani et al. 2006
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
What the sources say
- Not checked yetcites Flores and Herrero 2010
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
What the sources say
- Not checked yetcites Rippka et al. 1979
- Not checked yetcites Gugger and Hoffmann 2004
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Abstract
What the sources say
- Not checked yetcites Crowe et al. 2013
- Not checked yetcites Lyons et al. 2014
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In the paper
“Age ranges of specified and effective priors were similar, however, and could be accepted for the divergence time analyses.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Divergence time estimation
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In the paper
“For all analyses, accepted changes to the chains had values of approximately 30% at the time of convergence.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Ancestral character state reconstruction
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Material and methods > Restricting the origin of terminal cell differentiation (calibration 2)
What the sources say
- Not checked yetcites Bros et al. 1992
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Material and methods > Restricting the origin of cyanobacteria (calibration 1)
What the sources say
- Not checked yetcites Bekker et al. 2004
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In the paper
“All MCMC runs exhibited evidence of sufficient mixing.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Results > Ancestral character state reconstruction
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Material and methods > Restricting the origin of terminal cell differentiation (calibration 2)
What the sources say
- Not checked yetcites Horodyski and Donaldson 1980
- Not checked yetcites Golubic et al. 1995
- Not checked yetcites Srivastava 2005
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In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Material and methods > Restricting the origin of cyanobacteria (calibration 1)
What the sources say
- Not checked yetcites Planavsky et al. 2014
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Improved data set to reconstruct the evolutionary history of Cyanobacteria
What the sources say
- Not checked yetcites Schirrmeister et al. (2013)
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In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
What the sources say
- Not checked yetcites Kirschvink and Kopp 2008
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✗ Asserted: fails✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The authors may not put it forward as true. The paper’s conclusions may not depend on it. It may state two separate claims as one.
In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Comparison of cyanobacterial cell sizes to Precambrian microfossils
What the sources say
- Not checked yetcites Ohmoto et al. 2006
Strength:hedged· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“it comprises merely 1400 nucleotide sites with only half of them susceptible to change in phylum Cyanobacteria.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Improved data set to reconstruct the evolutionary history of Cyanobacteria
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In the paper
“Additionally, calibrations of tip clades have been claimed to be unsuitable for the accurate estimation of deep divergence events (Duchene et al. 2014).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Improved data set to reconstruct the evolutionary history of Cyanobacteria
What the sources say
- Not checked yetcites Duchene et al. 2014
Strength:hedged· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
What the sources say
- Not checked yetcites Nisbet et al. 2007
- Not checked yetcites Nisbet and Nisbet 2008
- Not checked yetcites Crowe et al. 2013
Strength:hedged· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Improved data set to reconstruct the evolutionary history of Cyanobacteria
What the sources say
- Not checked yetcites Shih and Matzke (2013)
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Comparison of cyanobacterial cell sizes to Precambrian microfossils
What the sources say
- Not checked yetcites Nisbet et al. 2007
- Not checked yetcites Nisbet and Fowler 2011
Strength:plain· not yet calibratedCausal:correlational· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Improved data set to reconstruct the evolutionary history of Cyanobacteria
What the sources say
- Not checked yetcites Iwabe et al. 1989
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Comparison of cyanobacterial cell sizes to Precambrian microfossils
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes? Based: unclearIt may state two separate claims as one.
- 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.
The paper states this without a source or data behind it here, so there is nothing to check it against. The quote shows it is in the paper.
In the paper
“Microfossils from Proterozoic and Archean deposits comprise multicellular forms, such as septate and non‐septate filaments, and unicellular remains, such as spheres and rods.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Comparison of cyanobacterial cell sizes to Precambrian microfossils
Strength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes? Load-bearing: unclear✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
What the sources say
- Not checked yetcites Kruschel and Castenholz 1998
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In Archean environments, Fe (II) toxicity could have prohibited oxygenic photosynthesis and subsequently allowed for only little oxygen production.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
In the paper
“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).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
What the sources say
- Not checked yetcites Catling and Claire 2005
Strength:plain· not yet calibratedCausal:direct· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passesProbably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Furthermore, multicellularity could have provided novel possibilities for cyanobacterial diversification and adaptation to new oxygenated habitats.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✗ Based: failsProbably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✗ Based: failsProbably not a substantial claim. The paper may give no reason why it holds.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Conclusion
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“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.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Conclusion
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes? Based: unclearIt may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Similarly, increased sizes of multicellular cyanobacteria may have resulted in higher metabolic rates, hence, higher photosynthetic activity and increased net oxygen production.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✗ Based: failsProbably not a substantial claim. The paper may give no reason why it holds. It may state two separate claims as one.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Additionally, multicellular growth may have provided competitive advantages that resulted in a higher growth success (Fig. 6).”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Discussion > Benefits of cyanobacterial multicellularity and its potential consequences for the GOE
Strength:hedged· not yet calibratedCausal:conditional· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✗ Based: failsProbably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Cyanobacteria originated in the mid‐Archean, long before the GOE, with multicellular taxa evolving towards the end of the Archean.”
§ Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils > Conclusion
Load-bearingStrength:plain· not yet calibratedTests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passesIt may state two separate claims as one.
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?
The cited source says what the claim attributes to it.
In the citing paper
“For example, cyanobacteria probably evolved [e.g., (3)] during this period”
From The Archean atmosphere (2020) · cites this paper as [3]
The cited source says what the claim attributes to it.
In the citing paper
“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”
Citations
Cites
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Flagged first, then by citations
4 of the 102 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Huisman, J., Codd, G. A., Paerl, H. W., Ibelings, B. W., Verspagen, J. M. H., & Visser, P. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0040-1 · Cited by 2,935
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Early photosynthetic eukaryotes inhabited low-salinity habitats
Sánchez‐Baracaldo, P., Raven, J. A., Pisani, D., & Knoll, A. H. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620089114 · Cited by 332
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“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
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The multicellular nature of filamentous heterocyst-forming cyanobacteria
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Oxidative Stress in Bacteria and the Central Dogma of Molecular Biology
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“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
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Solar energy conversion by photosystem II: principles and structures
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The possible evolution and future of CO2-concentrating mechanisms
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“…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).”
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Cyanobacterial evolution during the Precambrian
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Self-citationHorizontal gene transfer constrains the timing of methanogen evolution
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The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages
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Early Archean origin of Photosystem II
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“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 118
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Evolution of increased complexity and specificity at the dawn of form I Rubiscos
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Genetic responses to carbon and nitrogen availability in Anabaena
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Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA)
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“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
“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
“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
“…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
“…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
The Role of N 2 as a Geo-Biosignature for the Detection and Characterization of Earth-like Habitats
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
“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
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
“5 billion years ago in the predecessors to modern-day cyanobacteria [5].”
BackgroundHamilton, T. L. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.05.003 · Cited by 67
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
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
Bishé, B., Taton, A., & Golden, J. W. (2019) · iScience · doi:10.1016/j.isci.2019.09.002 · Cited by 55
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
“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 51
The origin and evolution of cyanobacteria
Shestakov, S. V., & Karbysheva, E. A. (2017) · Biology Bulletin Reviews · doi:10.1134/s2079086417040090 · Cited by 50
“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 46
“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 45
“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
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 45
“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
Zhao, L., Lin, L., Chen, M., et al. (2022) · Water Research · doi:10.1016/j.watres.2022.118385 · Cited by 43
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
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
“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
“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 41
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
Stadnichuk, I. N., & Kusnetsov, V. V. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032290 · Cited by 35
Electron transfer in biological systems
Marques, H. M. (2024) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-024-02076-8 · Cited by 43
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
Cyanobacteria in Terrestrial Symbiotic Systems
Rikkinen, J. K. (2017) · Springer eBooks · doi:10.1007/978-3-319-46261-5_8 · Cited by 38
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 36
“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
“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
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
“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
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 29
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 32
“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
“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
“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 30
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
“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 29
“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 28
“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 34
“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 23
Prebiotic Pathway from Ribose to RNA Formation
Bánfalvi, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22083857 · Cited by 26
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 26
Dvořák, P., Hašler, P., Casamatta, D. A., & Poulíčková, A. (2021) · Fottea · doi:10.5507/fot.2021.009 · Cited by 24
“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
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
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
Sultana, S., Awal, S., Shaika, N. A., & Khan, S. (2022) · Aquaculture Research · doi:10.1111/are.16011 · Cited by 25
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
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
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
“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
“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
Duval, C., Thomazeau, S., Drelin, Y., et al. (2018) · Harmful Algae · doi:10.1016/j.hal.2018.01.008 · Cited by 22
Ribose Selected as Precursor to Life
Bánfalvi, G. (2019) · DNA and Cell Biology · doi:10.1089/dna.2019.4943 · Cited by 23
“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
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
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
“…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
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
Demographic analysis of cyanobacteria based on the mutation rates estimated from an ancient ice core
Segawa, T., Takeuchi, N., Fujita, K., Aizen, V., Willerslev, E., & Yonezawa, T. (2018) · Heredity · doi:10.1038/s41437-017-0040-3 · Cited by 17
“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
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
“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
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
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
“…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
Ligrone, R. (2019) · Springer eBooks · doi:10.1007/978-3-030-16057-9_5 · Cited by 19
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
Metadata
- 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 › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › 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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