Origins of major archaeal clades correspond to gene acquisitions from bacteria

Abstract

The mechanisms that underlie the origin of major prokaryotic groups are poorly understood. In principle, the origin of both species and higher taxa among prokaryotes should entail similar mechanisms — ecological interactions with the environment paired with natural genetic variation involving lineage-specific gene innovations and lineage-specific gene acquisitions1,2,3,4. To investigate the origin of higher taxa in archaea, we have determined gene distributions and gene phylogenies for the 267,568 protein coding genes of 134 sequenced archaeal genomes in the context of their homologs from 1,847 reference bacterial genomes. Archaea-specific gene families define 13 traditionally recognized archaeal higher taxa in our sample. Here we report that the origins of these 13 groups unexpectedly correspond to 2,264 group-specific gene acquisitions from bacteria. Interdomain gene transfer is highly asymmetric, transfers from bacteria to archaea are more than 5-fold more frequent than vice versa. Gene transfers identified at major evolutionary transitions among prokaryotes specifically implicate gene acquisitions for metabolic functions from bacteria as key innovations in the origin of higher archaeal taxa.

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

“…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.…”

“…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. This might be because HGT-based prokaryotic recombination, as opposed to sex-based eukaryotic recombination, leads to chimeric pangenomes where individual genes frequently have different phylogenetic histories.…”

“…Here, we have improved our supertree implementation by correcting the likelihood calculations following the results of Bryant & Steel [49]. This new supertree method was implemented in the phylogenetic package P4 [50] and here we use this method to test Nelson-Sathi et al's [37] results with an independent methodological approach and a different dataset composed of 392 eubacterial and 51 archaebacterial taxa.…”

Erratum: Divergent functional isoforms drive niche specialisation for nutrient acquisition and use in rumen microbiome

“…Furthermore, the high frequency of horizontal gene transfer detected among bacteria (Gogarten et al, 1999;Creevey et al, 2004;Nelson-Sathi et al, 2014), even among 'core' genes (Creevey et al, 2011), suggests that horizontal gene transfer may also drive niche differentiation even within species (Coleman et al, 2006).…”