Metagenomics reveal unrestricted dispersal of extreme halophiles and higher connectivity among coastal vs. inland solar salterns and hypersaline lakes

Hypersaline environments constitute ideal systems for studying evolutionary processes and microbial diversification due to their relatively low (and thus tractable) diversity and geographically isolated nature. Based on metagenomic sequencing of samples from 25 hypersaline sites in 11 countries taken within a single year, we explored the relationships between environmental factors, geographic distance, and microbial community structure and diversification. Our results revealed that microbial communities of coastal sites were more similar to each other than those of the inland sites, reflecting higher connectivity due to ocean currents and nearly unrestricted dispersal. Conversely, inland hypersaline environments showed less connectivity and higher genetic and taxonomic dissimilarities that did not correlate with the distance between the sampled sites. The latter results reflect reduced species migration characterizing inland sites as well as site-specific environmental factors selecting for divergent taxa. The 484 MAGs recovered, representing 284 distinct species, revealed a striking global ubiquity, with 62.5% of the species showing cosmopolitanism, defined as being present at both coastal and inland sites. Most cosmopolitan species showed allopatric differentiation, reflected by an increased frequency of non-synonymous substitutions between MAGs of the same species recovered from more distant sites. However, a few cases of truly cosmopolitan genomovars (average nucleotide identity, or ANI > 99.8%), were also observed. Our results suggest that extreme halophiles have nearly unrestricted global dispersal among ocean-connected sites, and to a lesser extent, among geographically isolated inland sites, although cases of allopatric diversification were also observed.