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

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 Precambrian, cyanobacteria were one of the most important drivers of biological innovations, strongly impacting early Earth's environments. At the end of the Archean Eon, they were responsible for the rapid oxygenation of Earth's atmosphere during an episode referred to as the Great Oxidation Event (GOE). However, little is known about the origin and diversity of early cyanobacterial taxa, due to: (1) the scarceness of Precambrian fossil deposits; (2) limited characteristics for the identification of taxa; and (3) the poor preservation of ancient microfossils. Previous studies based on 16S rRNA 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 Precambrian 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 Archean 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.

On the origin of oxygenic photosynthesis and Cyanobacteria

“…Age estimates of the gene family of PSI and PSII (Cardona, 2018; are consistent with the geological record showing traces of oxygen throughout the Archean eon (4-2.5 Ba); these findings implied that oxygenic photosynthesis was already established by 3.0 Ba et al, 2014;Wang et al, 2018). 3), evolved towards the late Archean eon (Blank & S anchez-Baracaldo, 2010;Schirrmeister et al, 2015) or early Paleoproterozoic era (Shih et al, 2016). Furthermore, the standard heterodimeric photosystems, a defining trait of crown group Cyanobacteria (Fig.…”

“…New Phytologist ( The availability of new genomes and large-scale phylogenetic analyses have helped to resolve deep-branching relationships within Cyanobacteria, providing insights into the evolution of morphology and habitat within this phylum (Blank & S anchez-Baracaldo, 2010;Shih et al, 2013;Schirrmeister et al, 2015). Genomic data combined with advances in phylogenetic and trait evolution analyses have filled gaps in the geological record by providing testable hypotheses about the ancestral habitat of ancestral Cyanobacteria (Tomitani et al, 2006;Blank & S anchez-Baracaldo, 2010;Schirrmeister et al, 2016;S anchez-Baracaldo et al, 2017;Hammerschmidt et al, 2019).…”

Cyanobacterial ultrastructure in light of genomic sequence data

“…Previous studies have correlated morphological information with genomic sequence data. Schirrmeister et al (2015) demonstrated that multicellularity precedes the diversification of all modern cyanobacterial morphologies. Shih et al (2013) searched for genes responsible for morphological transitions between subsections but were unable to detect a specific gene set underlying any of the transitions.…”

“…The expanded coverage of cyanobacterial genome sequence data, and consequently improved phylogenetic trees, prompted the revisiting of questions about the evolution of cyanobacterial morphological features, for example the study of carbonate inclusions and polyphosphate bodies (Benzerara et al 2014) and of multicellularity in the phylum (Schirrmeister et al 2015). Similarly, the analysis of an extended pool of genes/genomes, together with the knowledge of the associated physiology, morphology, and ecology, has resulted in the discovery of previously unrecognized metabolic potential in cyanobacteria.…”

Cyanobacteria in Terrestrial Symbiotic Systems

“…The vegetative cells and heterocysts of Nostoc are mutually interdependent; the latter import photosynthates from vegetative cells and provide nitrogen in return. Multicellularity evolved in cyanobacteria already 2.5 billion years ago (Tomitani et al 2006;Schirrmeister et al 2011Schirrmeister et al , 2013Schirrmeister et al , 2015 and has since been lost and regained several times in different cyanobacterial lineages (Flores and Herrero 2010;Claessen et al 2014).…”