Abstract
What determines variation in genome size, gene content and genetic diversity at the broadest scales across the tree of life? Much of the existing work contrasts eukaryotes with prokaryotes, the latter represented mainly by Bacteria. But any general theory of genome evolution must also account for the Archaea, a diverse and ecologically important group of prokaryotes that represent one of the primary domains of cellular life. Here, we survey the extant diversity of Bacteria and Archaea, and ask whether the general principles of genome evolution deduced from the study of Bacteria and eukaryotes also apply to the archaeal domain. Although Bacteria and Archaea share a common prokaryotic genome architecture, the extant diversity of Bacteria appears to be much higher than that of Archaea. Compared with Archaea, Bacteria also show much greater genome-level specialisation to specific ecological niches, including parasitism and endosymbiosis. The reasons for these differences in long-term diversification rates are unclear, but might be related to fundamental differences in informational processing machineries and cell biological features that may favour archaeal diversification in harsher or more energy-limited environments. Finally, phylogenomic analyses suggest that the first Archaea were anaerobic autotrophs that evolved on the early Earth.
Highlights
One of the major challenges in evolutionary genetics is to explain the enormous variation in genome size and gene content across the tree of life in terms of basic evolutionary processes such as mutation, genetic drift and selection
The first Archaea were likely anaerobic autotrophs that lived on the early Earth
Their genomes were probably modestly smaller than those of extant Archaea
Summary
One of the major challenges in evolutionary genetics is to explain the enormous variation in genome size and gene content across the tree of life in terms of basic evolutionary processes such as mutation, genetic drift and selection. This extensive reductive evolution is predominantly seen in obligate, vertically transmitted intracellular symbionts: genome sizes of symbionts vary greatly and may even increase when compared with close free-living relatives [31] This testifies to many different evolutionary trajectories for the size and content of symbiont genomes depending on factors such as the life history of the symbiont and its transmission mode, and may help to make sense of the patterns observed for the genomes of archaeal symbionts. Most Archaea are not thermophiles, it is tempting to apply this line of reasoning more broadly, because adaptation to harsh conditions of other kinds — energy stress, low energy flux and extremes of pH — have been suggested to be a common feature shared across the archaeal domain [85] These hypotheses will remain speculative until more data on mutation rates and the distribution of fitness effects in Archaea inhabiting a broad variety of habitats become available. While some doubt over the ancestral genome size remains, these and other analyses suggest that the Wood–Ljungdahl pathway may have been the earliest carbon fixation pathway in the Archaea [48,93,94], supporting the view that LACA was an anaerobic autotroph
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