Background: The sulfur cycle encompasses a series of complex aerobic and anaerobic transformations of S-containing
molecules and plays a fundamental role in cellular and ecosystem-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, especially for inorganic sulfur compounds of intermediate oxidation states
(thiosulfate, tetrathionate, sulfite, polysulfides). Isolated and highly stratified, the extreme geochemical and environmental
features of meromictic ice-capped Lake A, in the Canadian High Arctic, provided an ideal model ecosystem to resolve the
distribution and metabolism of aquatic sulfur cycling microorganisms along redox and salinity gradients.
Results: Applying complementary molecular approaches, we identified sharply contrasting microbial communities and
metabolic potentials among the markedly distinct water layers of Lake A, with similarities to diverse fresh, brackish and saline
water microbiomes. Sulfur cycling genes were abundant at all depths and covaried with bacterial abundance. Genes for
oxidative processes occurred in samples from the oxic freshwater layers, reductive reactions in the anoxic and sulfidic
bottom waters and genes for both transformations at the chemocline. 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. Genes for the utilization of sulfur cycle intermediates were 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-oxidisers at the chemocline and by diverse microbial degraders of organic
sulfur molecules.
Conclusions: The 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 permanently stratified
lake extend the known diversity of microorganisms involved in sulfur transformations over a wide range of environmental
conditions. The results indicate that sulfur cycle intermediates and organic sulfur molecules are major sources of electron
donors and acceptors for aquatic and sedimentary microbial communities in association with the classical sulfur cycl