The Evolutionary Origins of Extreme Halophilic Archaeal Lineages

Yutian Feng, Uri Neri, Sean Gosselin, Artemis S. Louyakis, R. Thane Papke, Uri Gophna, Johann Peter Gogarten*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

Abstract

Interest and controversy surrounding the evolutionary origins of extremely halophilic Archaea has increased in recent years, due to the discovery and characterization of the Nanohaloarchaea and the Methanonatronarchaeia. Initial attempts in explaining the evolutionary placement of the two new lineages in relation to the classical Halobacteria (also referred to as Haloarchaea) resulted in hypotheses that imply the new groups share a common ancestor with the Haloarchaea. However, more recent analyses have led to a shift: the Nanohaloarchaea have been largely accepted as being a member of the DPANN superphylum, outside of the euryarchaeota; whereas the Methanonatronarchaeia have been placed near the base of the Methanotecta (composed of the class II methanogens, the Halobacteriales, and Archaeoglobales). These opposing hypotheses have far-reaching implications on the concepts of convergent evolution (distantly related groups evolve similar strategies for survival), genome reduction, and gene transfer. In this work, we attempt to resolve these conflicts with phylogenetic and phylogenomic data. We provide a robust taxonomic sampling of Archaeal genomes that spans the Asgardarchaea, TACK Group, euryarchaeota, and the DPANN superphylum. In addition, we assembled draft genomes from seven new representatives of the Nanohaloarchaea from distinct geographic locations. Phylogenies derived from these data imply that the highly conserved ATP synthase catalytic/noncatalytic subunits of Nanohaloarchaea share a sisterhood relationship with the Haloarchaea. We also employ a novel gene family distance clustering strategy which shows this sisterhood relationship is not likely the result of a recent gene transfer. In addition, we present and evaluate data that argue for and against the monophyly of the DPANN superphylum, in particular, the inclusion of the Nanohaloarchaea in DPANN.

Original languageEnglish
Article numberevab166
JournalGenome Biology and Evolution
Volume13
Issue number8
DOIs
StatePublished - 1 Aug 2021

Funding

FundersFunder number
National Science Foundation
National Aeronautics and Space Administration80NSSC18K1533, NNX15AM09G
Division of Molecular and Cellular Biosciences1716046
United States-Israel Binational Science FoundationBSF 2013061

    Keywords

    • Methanonatronarchaeia
    • Nanohaloarchaea
    • gene concordance
    • metagenomic-assembled genome (MAG)
    • single amplified genome (SAG)

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