Several independent adaptations of archaea to hypersaline environments

Abstract

Several archaeal lineages thrive in high, saturating salt concentrations. These extremely halophilic archaea, including Halobacteria, Nanohaloarchaeota, Methanonatronarchaeia, and Haloplasmatales, must maintain osmotic equilibrium with their environment. For this, they use a salt-in strategy, which involves pumping molar concentrations of potassium into the cells, which, in turn, has led to extensive proteome-wide modifications to prevent protein aggregation. However, the evolutionary history underlying these adaptations remains poorly understood. In particular, the number of times that these dramatic proteome-sweeping changes occurred is unclear due to the conflicting phylogenetic positions found for several of these lineages. Here, we present a resolved phylogeny of extremely halophilic archaea obtained using improved taxon sampling and state-of-the-art phylogenetic approaches designed to cope with the strong compositional biases of their proteomes. We describe two new uncultured lineages, Afararchaeaceae and Asboarchaeaceae, which break the long branches at the base of Haloarchaea and Nanohaloarchaeota, respectively. Our extensive phylogenomic analyses show that at least four independent adaptations to extreme halophily occurred during archaeal evolution. Finally, gene-tree/species-tree reconciliation suggests that gene duplication and horizontal gene transfer played an important role in this process, for example, by spreading key genes (such as those encoding potassium transporters) across the various extremely halophilic lineages.