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.

Keywords: atmosphere; divergence time estimation; early life; genomics; major transition.

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 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 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 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 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 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.