Metagenomics reveal allopatric speciation and higher connectivity among coastal vs. inland hypersaline lakes and solar salterns

Abstract

Hypersaline environments, due to their discrete and geographically isolated nature, constitute ideal systems for studying evolutionary patterns and microbial diversification, and especially here when contrasting coastal with inland systems. Based on metagenomic comparisons of 25 hypersaline sites across 11 countries, we explored the influence of environmental factors, ionic composition, and geographic distance on their microbial community structures and taxa diversification. Our results revealed that microbial communities from coastal environments were taxonomically and functionally more similar to each other than to those from inland sites. A distance-decay relationship in the genetic relatedness, significantly more pronounced for the coastal sites, was observed among reconstructed metagenome-assembled genomes (MAGs), clearer at distances below 400 km, but still detectable across global scales up to 20,000 km. The 484 MAGs recovered, representing 284 distinct species, revealed a striking global ubiquity, with 62.5% of the species showed cosmopolitanism as were detected across multiple sites. The higher taxonomic and genetic similarity of coastal environments over the inland sites seems to reflect an environmental connection that may be related to the ocean current dynamics. Most cosmopolitan species showed clear allopatric differentiation, although few cases of a single globally dominant genomovar (average nucleotide identity, ANI > 99.8%) were also observed, especially for some Haloquadratum species. The findings suggest that coastal hypersaline systems are loosely constrained by geographic isolation, with clear signals of allopatric speciation at the mesoscale (tenths to hundreds of kilometers) that become blurrier at larger scales.