Hikarchaeia demonstrate an intermediate stage in the methanogen-to-halophile transition

• Published in: Nature communications Vol. 11; no. 1; p. 5490
• Main Authors: Martijn, Joran, Schön, Max E., Lind, Anders E., Vosseberg, Julian, Williams, Tom A., Spang, Anja, Ettema, Thijs J. G.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 30.10.2020; Nature Publishing Group; Nature Portfolio
• Subjects: 631/326/26/2142; 631/326/26/2524; 631/326/26/2526; Aerobic respiration; Archaea; Genes; Genomes; Haloarchaea; Halophiles; Humanities and Social Sciences; Intermediates; Methanogenesis; Methanogenic bacteria; multidisciplinary; Science; Science (multidisciplinary)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-19200-2

Halobacteria (henceforth: Haloarchaea) are predominantly aerobic halophiles that are thought to have evolved from anaerobic methanogens. This remarkable transformation most likely involved an extensive influx of bacterial genes. Whether it entailed a single massive transfer event or a gradual stream of transfers remains a matter of debate. To address this, genomes that descend from methanogen-to-halophile intermediates are necessary. Here, we present five such near-complete genomes of Marine Group IV archaea (Hikarchaeia), the closest known relatives of Haloarchaea. Their inclusion in gene tree-aware ancestral reconstructions reveals an intermediate stage that had already lost a large number of genes, including nearly all of those involved in methanogenesis and the Wood-Ljungdahl pathway. In contrast, the last Haloarchaea common ancestor gained a large number of genes and expanded its aerobic respiration and salt/UV resistance gene repertoire. Our results suggest that complex and gradual patterns of gain and loss shaped the methanogen-to-halophile transition. A study of the first genomes of the marine Hikarchaeia, the closest known relatives of Haloarchaea, is presented. Their inclusion in ancestral reconstructions unveils an intermediate stage in the evolutionary transition from ancestral anaerobic methanogens to modern day aerobic halophiles.