Taxonomic and functional characterisation of viruses from a “lost world” in the Cuatro Ciénegas Basin, Mexico

Several lines of evidence suggest that the Cuatro Ciénegas Basin (CCB) is a “lost world” that has preserved at least some characteristics of ancient oceans. The microbial diversity of Archaean Domes (AD), a hypersaline and alkaline pond, includes various novel lineages of archaea and bacteria, as well as a highly diverse viral community. Nevertheless, the viruses from AD have not yet been subjected to a comprehensive taxonomic and functional characterisation. Given the pivotal role of viruses in microbial communities, we sought to determine which viruses are found at AD and the functions they encode, with the aim of identifying signatures of this so called “lost world”, and gaining deeper insights into how these viruses impact the structure of such unique microbial communities. The taxonomic classification of 87 metagenomic viral contigs (mVCs) from AD yielded taxonomic affiliations consistent with the environment, and with the diversity described in AD. We were able to identify signatures of the “lost world”, including associations with marine viruses, the formation of clusters of endemic viruses, and the detection of long branches between mVCs and their closest relatives. Furthermore, the high proportion of unannotated proteins and the low percentage of core genes indicate the distinctiveness of the viral lineages in AD. Finally, our functional characterisation indicated the presence of genes involved in diverse virus-host interactions, including metabolic reprogramming, evasion of anti-phage systems and superinfection exclusion. Intriguingly, we identified a mVC-encoded UDP-sulfoquinovose synthase (SQD1), an enzyme involved in sulfolipid biosynthesis, that has been described as an adaptation to low phosphorus concentrations in an endemic bacterium from the CCB. It is postulated that this enzyme, which was acquired by horizontal gene transfer from their hosts, may contribute to syntrophic interactions in this phosphorus-poor environment, where highly interdependent microorganisms have evolved.