Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea

Abstract

Archaebacterial halophiles (Haloarchaea) are oxygen-respiring heterotrophs that derive from methanogens-strictly anaerobic, hydrogen-dependent autotrophs. Haloarchaeal genomes are known to have acquired, via lateral gene transfer (LGT), several genes from eubacteria, but it is yet unknown how many genes the Haloarchaea acquired in total and, more importantly, whether independent haloarchaeal lineages acquired their genes in parallel, or as a single acquisition at the origin of the group. Here we have studied 10 haloarchaeal and 1,143 reference genomes and have identified 1,089 haloarchaeal gene families that were acquired by a methanogenic recipient from eubacteria. The data suggest that these genes were acquired in the haloarchaeal common ancestor, not in parallel in independent haloarchaeal lineages, nor in the common ancestor of haloarchaeans and methanosarcinales. The 1,089 acquisitions include genes for catabolic carbon metabolism, membrane transporters, menaquinone biosynthesis, and complexes I-IV of the eubacterial respiratory chain that functions in the haloarchaeal membrane consisting of diphytanyl isoprene ether lipids.LGT on a massive scale transformed a strictly anaerobic, chemolithoautotrophic methanogen into the heterotrophic, oxygen-respiring, and bacteriorhodopsin-photosynthetic haloarchaeal common ancestor.H alophilic archaebacteria (Haloarchaea) require concentrated salt solutions for survival and can inhabit saturated brine environments such as salt lakes, the Dead Sea, and salterns (1). In rRNA and phylogenomic analyses of informational genes, Haloarchaea always branch well within the methanogens (2-4). Haloarchaea can thus be seen as deriving from methanogen ancestors, but the physiology of methanogens and halophiles could hardly be more different. Methanogens are strict anaerobes, most species are lithoautotrophs that use electrons from H 2 to reduce CO 2 to methane (obligate hydrogenotrophic methanogens), thereby generating a chemiosmotic ion gradient for ATP synthesis in their energy metabolism, although some species can generate methane from reduced C 1 compounds, or acetate in the case of aceticlastic forms (5-7). Their carbon metabolism involves the Wood-Ljungdahl (acetyl-CoA) pathway of CO 2 fixation (5-7). In contrast, Haloarchaea are obligate heterotrophs that typically use O 2 as the terminal acceptor of their electron transport chain, although many can also use alternative electron acceptors such as nitrate in addition to light harnessing via a bacteriorhodopsin-based proton pumping system (8). The evolutionary nature of that radical physiological transformation from anaerobic chemolithoautotroph to aerobic heterotroph is of interest.Many individual reports document that lateral gene transfer (LGT) from eubacteria was involved in the origin of at least some components of haloarchaeal metabolism. These include the operon for gas vesicle formation, which allows Haloarchaea to remain in surface waters (9), the newly identified methylaspartate cycle of acetyl-CoA oxidation (10), vario...

Horizontal gene flow from Eubacteria to Archaebacteria and what it means for our understanding of eukaryogenesis

“…when eubacterial lineages are pruned out from PROK). Indeed, also in the previous supertree study of Pisani et al [5], nodes in Archaebacteria had higher support than nodes in Eubacteria, and Nelson-Sathi et al [36,37] pointed out that Archaebacteria are less prone than Eubacteria to engage in HGTs. However, how to interpret the tree in figure 5 in light of the tendency of Archaebacteria to engage in large-scale transfers from Eubacteria (and perhaps to Eubacteria) is far from obvious.…”

“…Nelson-Sathi et al [36,37] recently presented results suggesting that the emergence of several extant archaebacterial lineages correlates with several large inflows of genes acquired through massive, horizontal gene transfers (HGTs) from eubacterial donors (i.e. imports).…”

“…These imports (from Eubacteria to specific archaebacterial ancestors) were massive and may constitute signatures of ancient chromosomal recombination events. In the case of the Haloarchaea, Nelson-Sathi et al [36,37] concluded that these eubacterial genes were mainly imported from Actinobacteria. However, for other archaebacterial groups (Thermoproteales, Desulfurococcales, Methanobacteriales, Methanococcales and Methanosarcinales), the origins of which seem to have been preceded by extensive imports of eubacterial genes [37], a specific donor lineage could not be defined.…”

Insights into the metabolism, lifestyle and putative evolutionary history of the novel archaeal phylum ‘Diapherotrites’

“…The acquisition of bacterial genes was recently proposed as a driver of Halobacteriales evolution from a methanogenic ancestor (Nelson-Sathi et al, 2012). Within the eukaryotes, HGT has been shown to be important in the development of thermoacidophily and subsequent adaptation of the red algae Galdieria sulphuraria to hot acidic habitats (Qiu et al, 2013;Schönknecht et al, 2013), as well as the adaptation of gut fungi (Neocallimastigomycota) to the strict anaerobic, eutrophic and plant biomass-rich habitat in the herbivorous gut (Youssef et al, 2013).…”

An archaeal origin of eukaryotes supports only two primary domains of life

“…Given these considerations, the reversion to bacterialtype membranes in eukaryotes might be explained as part of the same process whereby ancestral archaeal pathways were replaced by bacterial equivalents to yield the metabolic similarities observed between Bacteria and contemporary eukaryotes [62][63][64][65]95,96,100 . This transition need not have greatly affected membrane function: in the Haloarchaea, which have obtained a large number of bacterial genes by HGT, transporters derived from Bacteria appear to function normally in the archaeal plasma membrane 101 .…”