Cited by 313Protist diversity and phylogenyPaleontology and Stratigraphy of FossilsPhotosynthetic Processes and Mechanisms

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Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils

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Abstract

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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Crossref · 10.1111/pala.12178

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Figures

Figure 1 Phylogenomic maximum likelihood tree. Phylogeny of 65 cyanobacterial taxa based on a supermatrix comprised of 756 concatenated protein sequences (197 761 amino acid sites). Maximum likelihood bootstrap support for clades is indicated at respective branches. Stars indicate 100% support calculated from 1000 bootstrap resamplings. Cyanobacterial taxa are colour‐coded. Unicellular taxa belonging to morphological subsections I and II are displayed in yellow and orange, respectively, whereas multicellular cyanobacterial taxa belonging to subsections III, IV and V are shown in green, blue and pink, respectively. The majority of branches in this phylogeny are well supported. Six distinct clades could be reconstructed with full support. Differentiated cyanobacteria belonging to subsections IV and V are the only groups where morphological and genomic data congruently suggest a monophyletic origin.
Figure 1 Phylogenomic maximum likelihood tree. Phylogeny of 65 cyanobacterial taxa based on a supermatrix comprised of 756 concatenated protein sequences (197 761 amino acid sites). Maximum likelihood bootstrap support for clades is indicated at respective branches. Stars indicate 100% support calculated from 1000 bootstrap resamplings. Cyanobacterial taxa are colour‐coded. Unicellular taxa belonging to morphological subsections I and II are displayed in yellow and orange, respectively, whereas multicellular cyanobacterial taxa belonging to subsections III, IV and V are shown in green, blue and pink, respectively. The majority of branches in this phylogeny are well supported. Six distinct clades could be reconstructed with full support. Differentiated cyanobacteria belonging to subsections IV and V are the only groups where morphological and genomic data congruently suggest a monophyletic origin.CC BY · PubMed Central
Figure 2 Description of the calibrations used in this study. Age restrictions apply to the origin of Cyanobacteria (calibration 1), the origin of cyanobacterial sections IV and V capable of cellular differentiation (calibration 2) and the origin of multicellularity within cyanobacteria (calibration 3). This study aims to test two hypotheses. Hypothesis 1: Multicellularity originated in cyanobacteria before the Great Oxidation Event (GOE), providing an advantage for cyanobacteria, resulting in higher abundance of those previously scarcely distributed prokaryotes, hence increasing oxygen production. Hypothesis 2: Multicellularity evolved after the GOE, as an adaptation to newly oxidized habitats that became available.
Figure 2 Description of the calibrations used in this study. Age restrictions apply to the origin of Cyanobacteria (calibration 1), the origin of cyanobacterial sections IV and V capable of cellular differentiation (calibration 2) and the origin of multicellularity within cyanobacteria (calibration 3). This study aims to test two hypotheses. Hypothesis 1: Multicellularity originated in cyanobacteria before the Great Oxidation Event (GOE), providing an advantage for cyanobacteria, resulting in higher abundance of those previously scarcely distributed prokaryotes, hence increasing oxygen production. Hypothesis 2: Multicellularity evolved after the GOE, as an adaptation to newly oxidized habitats that became available.CC BY · PubMed Central
Figure 3 Ancestral character state reconstruction to infer the evolution of multicellularity. Ancestral character states inferred from maximum likelihood analyses assuming asymmetrical transition rates between states were plotted on an ultrametric maximum likelihood tree of cyanobacteria. Pie charts on nodes display reconstructed ancestral character states, where black depicts multicellular and yellow unicellular growth states. Modern cyanobacterial taxa are displayed in coloured boxes, which indicate their taxonomic classification according to Rippka et al. (1979). Taxa belonging to unicellular subsections I and II are displayed with a yellow and orange background, respectively, whereas multicellular cyanobacteria from subsections III, IV and V are shown in green, blue and pink boxes, respectively. C1 and C2 refer to clades 1 and 2. Multicellularity evolved early during cyanobacterial history was lost several times and regained in two lineages.
Figure 3 Ancestral character state reconstruction to infer the evolution of multicellularity. Ancestral character states inferred from maximum likelihood analyses assuming asymmetrical transition rates between states were plotted on an ultrametric maximum likelihood tree of cyanobacteria. Pie charts on nodes display reconstructed ancestral character states, where black depicts multicellular and yellow unicellular growth states. Modern cyanobacterial taxa are displayed in coloured boxes, which indicate their taxonomic classification according to Rippka et al. (1979). Taxa belonging to unicellular subsections I and II are displayed with a yellow and orange background, respectively, whereas multicellular cyanobacteria from subsections III, IV and V are shown in green, blue and pink boxes, respectively. C1 and C2 refer to clades 1 and 2. Multicellularity evolved early during cyanobacterial history was lost several times and regained in two lineages.CC BY · PubMed Central
Figure 4 Prior and posterior age estimates for nodes that have been calibrated. User‐specified (grey) and effective prior age densities (red), as well as posterior age estimates (black) for the origin of cyanobacteria (calibration 1), the origin of sections IV and V cyanobacteria (calibration 2) and the origin of multicellularity (calibration 3). Compared are two hypotheses, each with (A, C) a wider (3.85–2.45 Ga) and (B, D) a narrower root calibration (3.85–2.958 Ga). The posterior age estimates for the origin of multicellularity (calibration 3) are in all cases shifted towards the older bound of the effective priors.
Figure 4 Prior and posterior age estimates for nodes that have been calibrated. User‐specified (grey) and effective prior age densities (red), as well as posterior age estimates (black) for the origin of cyanobacteria (calibration 1), the origin of sections IV and V cyanobacteria (calibration 2) and the origin of multicellularity (calibration 3). Compared are two hypotheses, each with (A, C) a wider (3.85–2.45 Ga) and (B, D) a narrower root calibration (3.85–2.958 Ga). The posterior age estimates for the origin of multicellularity (calibration 3) are in all cases shifted towards the older bound of the effective priors.CC BY · PubMed Central
Figure 5 Divergence time of cyanobacteria. Divergence times were reconstructed using a relaxed molecular clock. Two hypothesis have been tested, where multicellularity is assumed to have originated after the Great Oxidation Event (GOE; Hypothesis 1; A, B) or before the GOE (Hypothesis 2; C, D). The origin of cyanobacteria (root) was calibrated between the end of the late heavy bombardment and (A, C) the onset of the GOE, or (B, D) the first traces of oxygen at 2.958 Ga. In all four analyses, the cyanobacterial multicellularity is estimated to originate before the GOE. Nodes for calibrations 1–3 are marked in the first phylogenomic tree. Trees are ultrametric versions of the maximum likelihood tree presented in Figure 1. Colours refer to different morphological subsections of cyanobacteria. From top to bottom, the following taxa are displayed in each tree: (Clade 6) Leptolyngbya sp. PCC 7376, Synechococcus sp. PCC 7002, Cyanobacterium aponinum PCC 10605, Cyanobacterium stanieri PCC 7202, Synechocystis sp. PCC 6803 substrain PCC‐N, Cyanothece sp. PCC 7424, Microcystis aeruginosa NIES‐843, Cyanothece sp. PCC 8801, Crocosphaera watsonii WH 8501, Xenococcus sp. PCC 7305, Stanieria cyanosphaera PCC 7437, Gloeocapsa sp. PCC 73106, Halothece sp. PCC 7418, Dactylococcopsis salina PCC 8305, Spirulina subsalsa PCC 9445, Moorea producens 3L,Symploca sp. PCC 8002, Coleofasciculus chthonoplastes PCC 7420, Microcoleus sp. PCC 7113; Crinalium epipsammum PCC 9333, Chamaesiphon minutus PCC 6605; (Clade 5) ‘Nostoc azollae’ 0708, Cylindrospermopsis raciborskii CS‐505, Anabaena cylindrica PCC 7122, Cylindrospermum stagnale PCC 7417, Microchaete sp. PCC 7126, Anabaena variabilis ATTC 29413, Nostoc sp. PCC 7120, Nodularia spumigena CCY9414, Calothrix sp. PCC 6303, Fischerella muscicola PCC 7414, Fischerella thermalis PCC 7521, Chlorogloeopsis fritschii PCC 9212, Chlorogloeopsis fritschii PCC 6912, Mastigocladopsis repens PCC 10914, Chroococcidiopsis sp. PCC 8201, Chroococcidiopsis thermalis PCC 7203, Limnothrix redekei PCC 9416; (Clade 4) Arthrospira platensis NIES‐39, Arthrospira maxima CS‐328, Planktothrix agardhii NIVA‐CYA 34, Trichodesmium erythraeum IMS101, Microcoleus vaginatus FGP‐2, Oscillatoria nigro‐viridis PCC 7112; Geitlerinema sp. PCC 7407, Leptolyngbya sp. PCC 73110, Geitlerinema sp. PCC 8501, Nodosilinea nodulosa PCC 7104; (Clade 3) Synechococcus sp. WH 8102, Synechococcus sp. CC9605, Synechococcus sp. CC9311, Cyanobium gracile PCC 6307, Synechococcus elongatus PCC 6301, Prochlorothrix hollandica PCC 9006; (Clade 2) Acaryochloris marina MBIC11017, Acaryochloris sp. CCMEE 5410, Thermosynechococcus elongatus BP‐1; and (Clade 1) Pseudanabaena sp. PCC 7904, Pseudanabaena sp. PCC 7704, Synechocystis sp. PCC 9635, Pseudanabaena sp. PCC 7367; Synechococcus sp. JA‐3‐3Ab, Synechococcus sp. JA‐2‐3B'a(2‐13), Gloeobacter violaceus PCC 7421.
Figure 5 Divergence time of cyanobacteria. Divergence times were reconstructed using a relaxed molecular clock. Two hypothesis have been tested, where multicellularity is assumed to have originated after the Great Oxidation Event (GOE; Hypothesis 1; A, B) or before the GOE (Hypothesis 2; C, D). The origin of cyanobacteria (root) was calibrated between the end of the late heavy bombardment and (A, C) the onset of the GOE, or (B, D) the first traces of oxygen at 2.958 Ga. In all four analyses, the cyanobacterial multicellularity is estimated to originate before the GOE. Nodes for calibrations 1–3 are marked in the first phylogenomic tree. Trees are ultrametric versions of the maximum likelihood tree presented in Figure 1. Colours refer to different morphological subsections of cyanobacteria. From top to bottom, the following taxa are displayed in each tree: (Clade 6) Leptolyngbya sp. PCC 7376, Synechococcus sp. PCC 7002, Cyanobacterium aponinum PCC 10605, Cyanobacterium stanieri PCC 7202, Synechocystis sp. PCC 6803 substrain PCC‐N, Cyanothece sp. PCC 7424, Microcystis aeruginosa NIES‐843, Cyanothece sp. PCC 8801, Crocosphaera watsonii WH 8501, Xenococcus sp. PCC 7305, Stanieria cyanosphaera PCC 7437, Gloeocapsa sp. PCC 73106, Halothece sp. PCC 7418, Dactylococcopsis salina PCC 8305, Spirulina subsalsa PCC 9445, Moorea producens 3L,Symploca sp. PCC 8002, Coleofasciculus chthonoplastes PCC 7420, Microcoleus sp. PCC 7113; Crinalium epipsammum PCC 9333, Chamaesiphon minutus PCC 6605; (Clade 5) ‘Nostoc azollae’ 0708, Cylindrospermopsis raciborskii CS‐505, Anabaena cylindrica PCC 7122, Cylindrospermum stagnale PCC 7417, Microchaete sp. PCC 7126, Anabaena variabilis ATTC 29413, Nostoc sp. PCC 7120, Nodularia spumigena CCY9414, Calothrix sp. PCC 6303, Fischerella muscicola PCC 7414, Fischerella thermalis PCC 7521, Chlorogloeopsis fritschii PCC 9212, Chlorogloeopsis fritschii PCC 6912, Mastigocladopsis repens PCC 10914, Chroococcidiopsis sp. PCC 8201, Chroococcidiopsis thermalis PCC 7203, Limnothrix redekei PCC 9416; (Clade 4) Arthrospira platensis NIES‐39, Arthrospira maxima CS‐328, Planktothrix agardhii NIVA‐CYA 34, Trichodesmium erythraeum IMS101, Microcoleus vaginatus FGP‐2, Oscillatoria nigro‐viridis PCC 7112; Geitlerinema sp. PCC 7407, Leptolyngbya sp. PCC 73110, Geitlerinema sp. PCC 8501, Nodosilinea nodulosa PCC 7104; (Clade 3) Synechococcus sp. WH 8102, Synechococcus sp. CC9605, Synechococcus sp. CC9311, Cyanobium gracile PCC 6307, Synechococcus elongatus PCC 6301, Prochlorothrix hollandica PCC 9006; (Clade 2) Acaryochloris marina MBIC11017, Acaryochloris sp. CCMEE 5410, Thermosynechococcus elongatus BP‐1; and (Clade 1) Pseudanabaena sp. PCC 7904, Pseudanabaena sp. PCC 7704, Synechocystis sp. PCC 9635, Pseudanabaena sp. PCC 7367; Synechococcus sp. JA‐3‐3Ab, Synechococcus sp. JA‐2‐3B'a(2‐13), Gloeobacter violaceus PCC 7421.CC BY · PubMed Central
Figure 6 Illustration of cyanobacterial evolution leading towards the GOE. UV‐C radiation (below 290 nm) might have proved a major challenge for amotile unicellular cyanobacteria. The development of multicellularity will have provided two major advantages to a mat community: (1) the ability to move within the bacterial mat according to light requirements and/or lethal UV‐C avoidance; and (2) better attachment during the initial phase of mat development. These advantages of multicellularity in combination with the energetically higher efficiency of oxygenic photosynthesis may have led to a greater abundance of cyanobacterial‐dominated stromatolites and indirectly resulted in higher O 2 production towards the end of the Archean.
Figure 6 Illustration of cyanobacterial evolution leading towards the GOE. UV‐C radiation (below 290 nm) might have proved a major challenge for amotile unicellular cyanobacteria. The development of multicellularity will have provided two major advantages to a mat community: (1) the ability to move within the bacterial mat according to light requirements and/or lethal UV‐C avoidance; and (2) better attachment during the initial phase of mat development. These advantages of multicellularity in combination with the energetically higher efficiency of oxygenic photosynthesis may have led to a greater abundance of cyanobacterial‐dominated stromatolites and indirectly resulted in higher O 2 production towards the end of the Archean.CC BY · PubMed Central

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  • Probably not a substantial claim. 20
  • It may state two separate claims as one. 34
48 of 48
  • 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.”
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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
OpenAlex
W1831957949
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
Open access
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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