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Abstract
Cyanobacteria have exerted a profound influence on the progressive oxygenation of Earth. As a complementary approach to examining the geologic record—phylogenomic and trait evolutionary analyses of extant species can lead to new insights. We constructed new phylogenomic trees and analyzed phenotypic trait data using novel phylogenetic comparative methods. We elucidated the dynamics of trait evolution in Cyanobacteria over billion-year timescales, and provide evidence that major geologic events in early Earth’s history have shaped—and been shaped by—evolution in Cyanobacteria. We identify a robust core cyanobacterial phylogeny and a smaller set of taxa that exhibit long-branch attraction artifacts. We estimated the age of nodes and reconstruct the ancestral character states of 43 phenotypic characters. We find high levels of phylogenetic signal for nearly all traits, indicating the phylogeny carries substantial predictive power. The earliest cyanobacterial lineages likely lived in freshwater habitats, had small cell diameters, were benthic or sessile, and possibly epilithic/endolithic with a sheath. We jointly analyzed a subset of 25 binary traits to determine whether rates of trait evolution have shifted over time in conjunction with major geologic events. Phylogenetic comparative analysis reveal an overriding signal of decreasing rates of trait evolution through time. Furthermore, the data suggest two major rate shifts in trait evolution associated with bursts of evolutionary innovation. The first rate shift occurs in the aftermath of the Great Oxidation Event and “Snowball Earth” glaciations and is associated with decrease in the evolutionary rates around 1.8–1.6 Ga. This rate shift seems to indicate the end of a major diversification of cyanobacterial phenotypes–particularly related to traits associated with filamentous morphology, heterocysts and motility in freshwater ecosystems. Another burst appears around the time of the Neoproterozoic Oxidation Event in the Neoproterozoic, and is associated with the acquisition of traits involved in planktonic growth in marine habitats. Our results demonstrate how uniting genomic and phenotypic datasets in extant bacterial species can shed light on billion-year old events in Earth’s history.
Highlights
IntroductionSome questions remain over whether meaningful evolutionary inferences can be made over deep geologic timescales, especially due to the enormous billion-year time-spans separating extant species from their common ancestors and the potential for horizontal gene transfer [5, 6]
It is difficult to overstate the importance of Cyanobacteria in shaping the long-term biological and geological history of the Earth
Measured rates of lateral gene transfer among metabolic genes show these events occur only slowly and that most lateral gene transfer events appear to occur between closely related taxa and among taxa that inhabit common niches [13, 14], suggesting that comparative approaches to trait evolution using phylogenetic trees might be a profitable approach in these groups
Summary
Some questions remain over whether meaningful evolutionary inferences can be made over deep geologic timescales, especially due to the enormous billion-year time-spans separating extant species from their common ancestors and the potential for horizontal gene transfer [5, 6]. Measured rates of lateral gene transfer among metabolic genes show these events occur only slowly (with rates of up to 4.0 events per billion years; [12]) and that most lateral gene transfer events appear to occur between closely related taxa and among taxa that inhabit common niches [13, 14], suggesting that comparative approaches to trait evolution using phylogenetic trees might be a profitable approach in these groups
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