Low Rates of Lateral Gene Transfer among Metabolic Genes Define the Evolving Biogeochemical Niches of Archaea through Deep Time

Phylogenomic analyses of archaeal genome sequences are providing windows into the group's evolutionary past, even though most archaeal taxa lack a conventional fossil record. Here, phylogenetic analyses were performed using key metabolic genes that define the metabolic niche of microorganisms. Such genes are generally considered to have undergone high rates of lateral gene transfer. Many gene sequences formed clades that were identical, or similar, to the tree constructed using large numbers of genes from the stable core of the genome. Surprisingly, such lateral transfer events were readily identified and quantifiable, occurring only a relatively small number of times in the archaeal domain of life. By placing gene acquisition events into a temporal framework, the rates by which new metabolic genes were acquired can be quantified. The highest lateral transfer rates were among cytochrome oxidase genes that use oxygen as a terminal electron acceptor (with a total of 12-14 lateral transfer events, or 3.4-4.0 events per billion years, across the entire archaeal domain). Genes involved in sulfur or nitrogen metabolism had much lower rates, on the order of one lateral transfer event per billion years. This suggests that lateral transfer rates of key metabolic proteins are rare and not rampant.