Sulfur intermediates as new biogeochemical hubs in an aquatic model microbial ecosystem

Abstract BackgroundThe sulfur cycle encompasses a series of complex aerobic and anaerobic transformations of S-containing molecules, and plays a fundamental role in cellular and ecosystems level-processes, influencing biological carbon transfers and other biogeochemical cycles. Despite their importance, the microbial communities and metabolic pathways involved in these transformations remain poorly understood, notably for inorganic sulfur compounds of intermediate oxidation states (thiosulfate, tetrathionate, sulfite, polysulfides). Isolated and highly stratified, the extreme geochemical and environmental contexts of the meromictic ice-capped Lake A, in the Canadian High Arctic, provides an outstanding model ecosystem to resolve the distribution and metabolism of aquatic sulfur cycling microorganisms along redox and salinity gradients. ResultsApplying complementary molecular approaches, we identified sharply contrasting microbial communities and metabolic potentials among the distinct water layers of the Lake A, with homologies to diverse fresh, brackish and saline water microbiomes. Sulfur cycling genes were abundant at all depths, with oxidative processes in the oxic freshwater layers, reductive reactions in the anoxic and sulfidic bottom waters and genes for both transformations at the chemocline, and co-varied with bacterial abundance. Up to 154 different genomic bins with potential for sulfur transformation were recovered, revealing a panoply of taxonomically diverse microorganisms with complex metabolic pathways for biogeochemical sulfur reactions. Metabolism of sulfur cycle intermediates was widespread throughout the water column, co-occurring with sulfate reduction or sulfide oxidation pathways. The genomic bin composition suggested that in addition to chemical oxidation, these intermediate sulfur compounds were likely produced by the predominant sulfur chemo- and photo-oxidizers at the chemocline and by diverse microbial organic sulfur molecule degraders. ConclusionsThe Lake A microbial ecosystem provided an ideal opportunity to identify new features of the biogeochemical sulfur cycle. Our detailed metagenomic analyses across the broad physico-chemical gradients of this highly stratified lake extend the known diversity of microorganisms and metabolic pathways involved in sulfur transformations over a wide range of environmental conditions. The results identify the importance of sulfur cycle intermediates and organic sulfur molecules as major sources of electron donors and acceptors for aquatic and sedimentary microbial communities in association with the classical sulfur cycle.