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

The DOI matches its Crossref record; 98 of the 102 references it cites were found in a registry or an index; none of the 90 sources its claims cite is checked for support yet.

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

Open access

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.

Overview

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Written from the paper’s full text.

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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Integrity signals

Registry

Crossref · 10.1111/pala.12178

Cites

98 of 98 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

0 of 90 cited sources checked · 0 supported · 0 flagged

Show all 76 claims

  • 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.”
5 of 5

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?

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

    Major

    The 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.

  • Root-calibration assignments are reversed

    Major

    The 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.

  • Supermatrix length changes in the discussion

    Minor

    The discussion reports 197,766 amino acid sites, while the methods report 197,761 for the same supermatrix.

  • Five stated multicellular strains are six listed strains

    Minor

    The 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.

  • Figure captions give a different narrow root bound

    Minor

    The figure caption gives 2.958 Ga as the lower bound of the narrow root calibration, whereas Table 1 gives 2.918 Ga.

  • q01 is assigned to both opposing transitions

    Minor

    The 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.

  • Western Australian deposit is dated in Ma instead of Ga

    Minor

    The 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.

  • Figure 2 reverses the hypothesis labels

    Minor

    Figure 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.

8 of 8

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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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