Phylogenetic analyses of conserved core genes have disentangled most of the ancient relationships in Archaea. However, some groups remain debated, like the DPANN, a deep-branching super-phylum composed of nanosized archaea with reduced genomes. Among these, the Nanohaloarchaea require high-salt concentrations for growth. Their discovery in 2012 was significant because they represent, together with Halobacteria (a Class belonging to Euryarchaeota), the only two described lineages of extreme halophilic archaea. The phylogenetic position of Nanohaloarchaea is highly debated, being alternatively proposed as the sister-lineage of Halobacteria or a member of the DPANN super-phylum. Pinpointing the phylogenetic position of extreme halophilic archaea is important to improve our knowledge of the deep evolutionary history of Archaea and the molecular adaptive processes and evolutionary paths that allowed their emergence. Using comparative genomic approaches, we identified 258 markers carrying a reliable phylogenetic signal. By combining strategies limiting the impact of biases on phylogenetic inference, we showed that Nanohaloarchaea and Halobacteria represent two independent lines that derived from two distinct but related methanogen Class II lineages. This implies that adaptation to high salinity emerged twice independently in Archaea and indicates that emergence of Nanohaloarchaea within DPANN in previous studies is likely the consequence of a tree reconstruction artifact, challenging the existence of this super-phylum.
Previous reports have shown that environmental temperature impacts proteome evolution in Bacteria and Archaea. However, it is unknown whether thermoadaptation mainly occurs via the sequential accumulation of substitutions, massive horizontal gene transfers, or both. Measuring the real contribution of amino acid substitution to thermoadaptation is challenging, because of confounding environmental and genetic factors (e.g. pH, salinity, genomic G+C content) that also affect proteome evolution. Here, using Methanococcales, a major archaeal lineage, as a study model, we show that optimal growth temperature is the major factor affecting variations in amino acid frequencies of proteomes. By combining phylogenomic and ancestral sequence reconstruction approaches, we disclose a sequential substitutional scheme in which lysine plays a central role by fine tuning the pool of arginine, serine, threonine, glutamine, and asparagine, whose frequencies are strongly correlated with optimal growth temperature. Finally, we show that colonization to new thermal niches is not associated with high amounts of horizontal gene transfers. Altogether, while the acquisition of a few key proteins through horizontal gene transfer may have favoured thermoadaptation in Methanococcales, our findings support sequential amino acid substitutions as the main factor driving thermoadaptation.
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