Timing of morphological and ecological innovations in the cyanobacteria – a key to understanding the rise in atmospheric oxygen

Abstract

When cyanobacteria originated and diversified, and what their ancient traits were, remain critical unresolved problems. Here, we used a phylogenomic approach to construct a well-resolved 'core' cyanobacterial tree. The branching positions of four lineages (Thermosynechococcus elongatus, Synechococcus elongatus, Synechococcus PCC 7335 and Acaryochloris marina) were problematic, probably due to long branch attraction artifacts. A consensus genomic tree was used to study trait evolution using ancestral state reconstruction (ASR). The early cyanobacteria were probably unicellular, freshwater, had small cell diameters, and lacked the traits to form thick microbial mats. Relaxed molecular clock analyses suggested that early cyanobacterial lineages were restricted to freshwater ecosystems until at least 2.4 Ga, before diversifying into coastal brackish and marine environments. The resultant increases in niche space and nutrient availability, and consequent sedimentation of organic carbon into the deep oceans, would have generated large pulses of oxygen into the biosphere, possibly explaining why oxygen rose so rapidly. Rapid atmospheric oxidation could have destroyed the methane-driven greenhouse with simultaneous drawdown in pCO(2), precipitating 'Snowball Earth' conditions. The traits associated with the formation of thick, laminated microbial mats (large cell diameters, filamentous growth, sheaths, motility and nitrogen fixation) were not seen until after diversification of the LPP, SPM and PNT clades, after 2.32 Ga. The appearance of these traits overlaps with a global carbon isotopic excursion between 2.2 and 2.1 Ga. Thus, a massive re-ordering of biogeochemical cycles caused by the appearance of complex laminated microbial communities in marine environments may have caused this excursion. Finally, we show that ASR may provide an explanation for why cyanobacterial microfossils have not been observed until after 2.0 Ga, and make suggestions for how future paleobiological searches for early cyanobacteria might proceed. In summary, key evolutionary events in the microbial world may have triggered some of the key geologic upheavals on the Paleoproterozoic Earth.

Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

“…The topology of the reconstructed tree is consistent with previous phylogenomics results (21,22) and is identical to the unrooted topology obtained for the concatenate of 474 near universal single copy genes (PHYML, LG+Γ8+I) and the consensus tree of 364 universal single copy trees (using both PHYML, LG+Γ8+I and TreeFinder, WAG+Γ8+I trees). The topology differs from two recent studies with different (23) or larger (24) species sampling than ours: in ref.…”

“…Comparing the reconstructed relative chronology with two recent molecular dating studies by Falcon et al (23) and Blank et al (22), we find good agreement for early chronological relationships: both find that node 4, the ancestor of nodes 5 (clade containing Trichodesmium and Nostocales) and 6 (clade containing Synchocystis and Microcystis) is the first major group to emerge; both also support the order of nodes 5, 6, and 8, as well as the late diversification of the Synechococcus-Prochlorococcus group (nodes 13-15 and 17); this correspondence with our results is remarkable given that both studies rely on a relaxed molecular clock and calibration constraints based on the geological and The maximum likelihood time orders are indicated as node labels. Squares correspond to major diversification events discussed in the text.…”

“…Cyanobacteria are distinguished among prokaryotes by a relative abundance of microfossil and biomarker records (29). However, even this relative abundance reduces to a handful calibration points for the timing of cyanobacterial evolution: (i) the presence of free oxygen in late Archean oceans (30) and the rapid rise in atmospheric oxygen 2.45-2.32 billion years ago (Ga) (31) is attributed to cyanobacteria (32), but many details of these associations continue to be investigated (33,34); (ii) unambiguous microfossil evidence dates to ∼2.0 Ga, by which time diversification was advanced with fossils of filamentous forms dating from 1.9 Ga (35) and akinete forming Cyanobacteria from 2.1 Ga (29); and (iii) by 1.4 Ga diversification of major extant morphologically distinguishable lineages was complete (22,36).…”

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

“…This is also presumed to be the case for Earth's more distant past with respect to photosynthetic bacteria, though perhaps to a lesser magnitude (Blank & Sanchez‐Baracaldo, 2010). However, the ability to resolve details about this distant past (specifically, when Rubisco‐mediated carbon uptake evolved or how efficiently ancestral Rubisco proteins functioned under ancient environmental conditions) are limited by the scant traces of geological and paleobiological evidence that survive from that history (Benton, Wills, & Hitchin, 2000; Braakman & Smith, 2012; Knoll, Javaux, Hewitt, & Cohen, 2006).…”

Algal evolution in relation to atmospheric CO 2 : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

“…Eukaryotic algae have occurred since at least 1.2 Ga [2][3][4] and from freshwaters, and possibly lake margins, since 1.1 Ga [5] (table 1). Since 2.4 Ga, the biosphere has become increasingly oxygenated [1], reflecting the colonization of the oceans by cyanobacteria after their origin in freshwater habitats, with a corresponding increase in the capacity of these organisms to have global biogeochemical influence [15,16] (table 1). A significant increase in oxygen, with oxygenation of the deep ocean, occurred in the Neoproterozoic 0.54-1 Ga [32], with variations in the Phanaerozoic including the highest known level in the Permo-Carboniferous glaciation [33].…”