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A Genomic Timescale of Prokaryote Evolution: Insights Into the Origin of Methanogenesis, Phototrophy, and the Colonization of Land

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A Genomic Timescale of Prokaryote Evolution: Insights Into the Origin of Methanogenesis, Phototrophy, and the Colonization of Land

Fabia U Battistuzzi et al. BMC Evol Biol.

Abstract

Background: The timescale of prokaryote evolution has been difficult to reconstruct because of a limited fossil record and complexities associated with molecular clocks and deep divergences. However, the relatively large number of genome sequences currently available has provided a better opportunity to control for potential biases such as horizontal gene transfer and rate differences among lineages. We assembled a data set of sequences from 32 proteins (approximately 7600 amino acids) common to 72 species and estimated phylogenetic relationships and divergence times with a local clock method.

Results: Our phylogenetic results support most of the currently recognized higher-level groupings of prokaryotes. Of particular interest is a well-supported group of three major lineages of eubacteria (Actinobacteria, Deinococcus, and Cyanobacteria) that we call Terrabacteria and associate with an early colonization of land. Divergence time estimates for the major groups of eubacteria are between 2.5-3.2 billion years ago (Ga) while those for archaebacteria are mostly between 3.1-4.1 Ga. The time estimates suggest a Hadean origin of life (prior to 4.1 Ga), an early origin of methanogenesis (3.8-4.1 Ga), an origin of anaerobic methanotrophy after 3.1 Ga, an origin of phototrophy prior to 3.2 Ga, an early colonization of land 2.8-3.1 Ga, and an origin of aerobic methanotrophy 2.5-2.8 Ga.

Conclusions: Our early time estimates for methanogenesis support the consideration of methane, in addition to carbon dioxide, as a greenhouse gas responsible for the early warming of the Earths' surface. Our divergence times for the origin of anaerobic methanotrophy are compatible with highly depleted carbon isotopic values found in rocks dated 2.8-2.6 Ga. An early origin of phototrophy is consistent with the earliest bacterial mats and structures identified as stromatolites, but a 2.6 Ga origin of cyanobacteria suggests that those Archean structures, if biologically produced, were made by anoxygenic photosynthesizers. The resistance to desiccation of Terrabacteria and their elaboration of photoprotective compounds suggests that the common ancestor of this group inhabited land. If true, then oxygenic photosynthesis may owe its origin to terrestrial adaptations.

Figures

Figure 1
Figure 1
Phylogenetic tree (ME; α = 0.94) of eubacteria rooted with archaebacteria, using sequences of 32 proteins (7,597 amino acids). Bootstrap values are shown on nodes; asterisks indicate support values > 95%. For major groups, support values from three phylogenetic methods (ME/ML/Bayesian) are indicated in italics (dash indicates a group was not present).
Figure 2
Figure 2
Phylogenetic tree (ME; α = 1.20) of archaebacteria rooted with eubacteria, using sequences of 32 proteins (7,338 amino acids). Bootstrap values are shown on nodes; asterisks indicate support values > 95%. For major groups, support values from three phylogenetic methods (ME/ML/Bayesian) are indicated in italics.
Figure 3
Figure 3
A timescale of prokaryote evolution. Letters indicate nodes discussed in the text. The last common ancestor was arbitrarily placed at 4.25 Ga in the tree, although this placement was not part of the analyses. The grey rectangle shows the time prior to the initial rise in oxygen (presumably anaerobic conditions). Mtb: Methanothermobacter, Tab: Thermoanaerobacter, Tsc: Thermosynechococcus.
Figure 4
Figure 4
A time line of metabolic innovations and events on Earth. The minimum time for oxygenic photosynthesis is constrained by the Great Oxidation Event (2.3 Ga) whereas the maximum time for the origin of life is constrained by the origin of Earth (4.5 Ga). Horizontal lines indicate credibility intervals, white boxes indicate minimum and maximum time constraints on the origin of a metabolism or event, and colored boxes indicate the presence of the metabolism or event.

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