Sulfide-oxidizing potential and hypersalinity tolerance strategies in salt-crust covered coastal microbial mats

Hypersaline microbial mats are dense microbial ecosystems capable of performing nearly complete element cycling under harsh conditions including near-saturation salinity. Our previous study of salt-crust-covered microbial mats showed that oxygenic photosynthesis was inhibited at salt saturation, while phototrophic sulfide oxidation persisted despite well-known sulfide-oxidizing taxa being undetectable. In this study, we analyzed metagenome-assembled genomes (MAGs) from the same mats to identify sulfide-oxidizing taxa and adaptations enabling oxygenic phototrophs to survive salt saturation. We extended the dataset by including morphologically identical mats exposed to lower salinity regimes to identify metabolic capabilities specifically selected for by saturation-level salinity. The phototrophic sulfide oxidation capability was found in nearly all cyanobacterial MAGs, in some Chloroflexota, and in abundant Rhodovibrio populations previously not known to oxidize sulfide. Furthermore, we found clear indications of Haloarchaea-like potassium-based osmoregulation in Bradymonadaceae (Myxococcota) adding another taxon to the few known potassium-accumulating bacteria. Despite lower oxygen concentrations, salt-crust-covered mats showed smaller proportions of fermenters and higher proportions of aerobic microorganisms than lower-salinity mats. We compared the genetic signatures of hypersalinity and desiccation tolerance in cyanobacterial MAGs from this study to genomes from desiccation-prone environments such as desert soils and small freshwater streams. Genomes of hyperhalophilic cyanobacteria were characterized by lack of certain potassium transporters and catalase genes and presence of additional osmolyte transporter subunits and sulfide-oxidation genes. We hypothesize that during salt saturation the oxidative stress for mat dwelling cyanobacteria is lowered, while the ability to oxidize sulfide provides them with energy when oxygenic photosynthesis is inhibited.