Global dominance of Haloquadratum walsbyi by a single genomovar with distinct gene content and viral cohorts from close relatives

Abstract

Haloquadratum walsbyi is generally the dominant species in hypersaline ecosystems at salt saturation conditions. Here, we followed the dynamics of its genomovars and associated viruses during recurrent evaporation-dilution disturbances of varying intensities at the mesocosm scale over 813 days. The diversity observed within a single mesocosm was also compared with that in a global-scale inventory of hypersaline environments of thalassohaline origin. The 140 binned metagenome assembled genomes (MAGs) together with the genomes of the (only) two available of H. walsbyi isolates grouped into four highly related (98.25% > Average Nucleotide Identity [ANI] > 99.5%) dominant genomovars (intra-genomovar ANI > 99.5%). In mesocosm experiments, moderate disturbances (i.e. recurrent dilution from saturation to 20% salts) enhanced the abundance of the already-dominant genomovar Hqrw1, resulting in reduced intraspecific diversity. This genomovar also dominated in almost all sites sampled around the globe. In contrast, more intense disturbance (i.e. recurrent dilution from saturation to 13% salts) decreased the abundance of Hqrw1 to lower levels than genomovar Hqrw2 by the end of the incubation, which seems to resist better osmotic changes. Further, our results showed that genomovars were followed by their viral cohorts, who play a significant role in the global dominance of the four H. walsbyi genomovars and their replacement under unfavorable conditions. We propose that the global dominance of H. walsbyi in thalassohaline hypersaline sites is enabled by both the success of Hqrw1 in high but stable salinities and the larger resistance of Hqrw2 to extreme osmotic stress, safeguarding the presence of the species in the system.