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

Abstract

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.

Geological and Geochemical Constraints on the Origin and Evolution of Life

“…Numerous closely related organisms may survive a bottleneck, further fuzzing the tree. Biologists have constructed deep trees that account for horizontal transfer (Abby et al, 2012;Blank, 2012;Puigbò et al, 2013). Nearly universal trees exist, implying that nodes are fuzzy though useful constructs; the standard tree with LUCA branching to the domains of bacteria and archaea is likely correct (Abby et al, 2012;Puigbò et al, 2013).…”

Descent of Bacteria and Eukarya from an archaeal root of life

“…A ToL of transfer RNAs based on the genetic distances between the 20 classes of tRNA acceptors for different amino acids located its root near the hyperthermophilic archaeal methanogen Methanopyrus (Mka) 2 . Although this rooting is supported by a wide range of evidence 3–9 , and the age of ~2.7 Gya for the Methanopyrus lineage as the oldest among living organisms 10 , the phylogenies of the three biological domains are beset by two fundamental problems: viz. the uncertain relationship between Archaea and Bacteria, and the identity of the prokaryotic-parent that underwent genome merger with an alphaproteobacterium to give rise to Eukarya.…”

“…Addressing the inadequacy of ESP coverage by single archaeal species 29,30 , it was suggested that HGTs, or development of phagocytosis by an ESP-rich archaeon might provide a solution 26,31 . However, the frequencies of HGTs might be a limiting factor 10,32 , and rProts could be particularly resistant to HGT 33 .…”

Microbial dynamics in a thawing world: Microbial ecology of a permafrost active layer

“…Hydrogenotrophic methanogenesis, though yielding low energy, is one of the oldest extant energy pathways (Sousa and Martin, 2014) being the main contender for the ancestral metabolism of Euryarchaea (> 2.7 Bya) (Blank, 2012) but with biogeochemical evidence dating it at over 3.4 Bya (Ueno et al, 2006). The acquisition of bacterial cytochromes and novel acetate activation pathways enabling use of acetate as the electron acceptor in methanogenesis occurred recently, most likely around 0.5 Bya years ago (Fournier and Gogarten, 2008;Blank, 2012).…”

“…The acquisition of bacterial cytochromes and novel acetate activation pathways enabling use of acetate as the electron acceptor in methanogenesis occurred recently, most likely around 0.5 Bya years ago (Fournier and Gogarten, 2008;Blank, 2012). Cytochromes are present in Methanocella spp.…”