pubmed.ncbi.nlm.nih.gov

The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages - PubMed

  • ️Fri Jan 01 2021

The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages

G P Fournier et al. Proc Biol Sci. 2021.

Abstract

The record of the coevolution of oxygenic phototrophs and the environment is preserved in three forms: genomes of modern organisms, diverse geochemical signals of surface oxidation and diagnostic Proterozoic microfossils. When calibrated by fossils, genomic data form the basis of molecular clock analyses. However, different interpretations of the geochemical record, fossil calibrations and evolutionary models produce a wide range of age estimates that are often conflicting. Here, we show that multiple interpretations of the cyanobacterial fossil record are consistent with an Archean origin of crown-group Cyanobacteria. We further show that incorporating relative dating information from horizontal gene transfers greatly improves the precision of these age estimates, by both providing a novel empirical criterion for selecting evolutionary models, and increasing the stringency of sampling of posterior age estimates. Independent of any geochemical evidence or hypotheses, these results support oxygenic photosynthesis evolving at least several hundred million years before the Great Oxygenation Event (GOE), a rapid diversification of major cyanobacterial lineages around the time of the GOE, and a post-Cryogenian origin of extant marine picocyanobacterial diversity.

Keywords: Archean; Cryogenian; Great Oxygenation Event; cyanobacteria; horizontal gene transfer; molecular clock.

PubMed Disclaimer

Figures

Figure 1.
Figure 1.

Posterior age distributions of crown Cyanobacteria using different sets of fossil calibrations. Model labels are as specified in table 1 and electronic supplementary material, table S3: BA = Obruchevella + Eohyella (orange); BB = Obruchevella + Eohyella + plastid (blue); BE = Obruchevella + Eohyella + plastid + Eoentophysalis (red); BI = Obruchevella + endolithic (purple); BJ = Obruchevella + endolithic + plastid (black). All ages shown are for the CIR_nobd evolutionary model.

Figure 2.
Figure 2.

Chronogram of cyanobacteria. Grey bars show uncertainty (95% CI) under the CIR_nobd model using the BE calibration schema. HGT-constrained age estimates for each node are additionally included (black dashes indicate mean ages, purple bars indicate 95% CI uncertainty ranges). Major non-cyanobacterial clades are collapsed (grey triangles). Numbers indicate nodes of fossil calibrations (electronic supplementary material, table S2). Background colours represent Archean (red), Proterozoic (orange) and Phanerozoic (yellow) eons. The older and younger-bounds for the cyanobacterial stem lineage are indicated by dotted lines.

Figure 3.
Figure 3.

Divergence time estimates for major nodes in cyanobacterial evolution. (a) Crown bacteria (root); (b) total group Cyanobacteria; (c) crown Cyanobacteria; (d) total group marine SynPro. Prior (dashed) and posterior (solid) age distributions are shown. The root prior (black) is shown for crown bacteria (a). Age distributions are shown for the following analyses: uncalibrated (blue); calibration schemas excluding cyanobacterial/plastid calibrations (BH, purple); and including the cyanobacterial calibrations (BE, orange). Additionally, HGT-constrained age distributions are shown (red).

Figure 4.
Figure 4.

Proposed narrative for the cyanobacterial context of Earth's oxidation. Relative probability density distributions are shown for crown bacteria (purple), total group Cyanobacteria (red) and crown group Cyanobacteria (blue). This hypothesized history of cyanobacteria shows oxygenic forms arising from within a diversity of anoxygenic stem groups in the Archean. A timeline of geological evidence shows that these dates are consistent with Mesoarchaean and Neoarchaean geochemical and morphological evidence of oxygenic photosynthesis (detailed in electronic supplementary material, text S5).

Similar articles

Cited by

References

    1. Martin WF, Bryant DA, Beatty JT. 2018A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiol. Rev. 42, 205-231. (10.1093/femsre/fux056) - DOI - PMC - PubMed
    1. Lyons TW, Reinhard CT, Planavsky NJ. 2014The rise of oxygen in Earth's early ocean and atmosphere. Nature 506, 307-315. (10.1038/nature13068) - DOI - PubMed
    1. Buick R. 1992The antiquity of oxygenic photosynthesis: evidence from stromatolites in sulphate-deficient Archaean lakes. Science 255, 74-77. (10.1126/science.11536492) - DOI - PubMed
    1. Sim MS, Liang B, Petroff AP, Evans A, Klepac-Ceraj V, Flannery DT, Walter MR, Bosak T. 2012Oxygen-dependent morphogenesis of modern clumped photosynthetic mats and implications for the Archean stromatolite record. Geosciences 2, 235-259. (10.3390/geosciences2040235) - DOI
    1. Flannery DT, Walter MR. 2012Archean tufted microbial mats and the Great Oxidation Event: new insights into an ancient problem. Aust. J. Earth Sci. 59, 1-11. (10.1080/08120099.2011.607849) - DOI

Publication types

MeSH terms

Substances

LinkOut - more resources