Origins of major archaeal clades correspond to gene acquisitions from bacteria

• Published in: Nature (London) 2015-01, Vol.517 (7532), p.77-80
• Main Authors: Nelson-Sathi, Shijulal, Sousa, Filipa L., Roettger, Mayo, Lozada-Chávez, Nabor, Thiergart, Thorsten, Janssen, Arnold, Bryant, David, Landan, Giddy, Schönheit, Peter, Siebers, Bettina, McInerney, James O., Martin, William F.
• Format: Article
• Language: English
• Subjects: 42; 45; 631/181/735; Archaea - classification; Archaea - genetics; Archaea - metabolism; Archaeabacteria; Archaeal Proteins - genetics; Bacteria; Bacteria - genetics; Bacteria - metabolism; Evolution, Molecular; Gene Transfer, Horizontal - genetics; Genes; Genes, Archaeal - genetics; Genes, Bacterial - genetics; Genetic aspects; Genetic diversity; Genome, Archaeal - genetics; Genomes; Humanities and Social Sciences; Innovations; letter; Metabolism; multidisciplinary; Origin; Phylogeny; Prokaryotes; Science; Taxa; Taxonomy
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature13805

A comparison of protein-coding genes from 134 archaeal genomes with their homologues in 1,847 bacterial genomes reveals that, during evolution, genes are transferred more often from bacteria to archaea than vice versa, and that gene influxes from bacteria can bring about the origin of major archaeal groups. Gene imports crucial in archaeal evolution Lateral (or horizontal) gene transfer between individual cells is recognized as an important factor in genome evolution and species formation in prokaryotes such as cyanobacteria and proteobacteria. This study of gene of distribution and phylogenies in 134 archaeal genomes shows that origins of the 13 traditionally recognized higher taxa in the archaea correspond to 2,264 group-specific lateral gene acquisitions from bacteria. Transfers from bacteria to archaea are more than fivefold more frequent than vice versa. Gene acquisitions for metabolic functions from bacteria represent key innovations in the origin of higher archaeal taxa. 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 acquisitions 1 , 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 homologues from 1,847 reference bacterial genomes. Archaeal-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 fivefold 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.