Use of metagenomics and metatranscriptomics to determine the influence of organic sulfur compounds on the sulfur cycle in the sediment of a low-sulfate freshwater system

Abstract

The sulfur cycle is an important and complex biogeochemical cycle involving both inorganic and organic species in both oxic and anoxic environments. However, due to the lack of research regarding the sulfur cycle in freshwater systems, the contributions of organic sulfur compounds to the sulfur cycle are underappreciated. Recent studies have suggested organic sulfur compounds likely fuels sulfate reduction, especially in low-sulfate oligotrophic freshwater systems, through a possible cryptic sulfur cycle. To determine the contributions that organic sulfur compounds may have in this environment, we used Lake Superior sediment to analyze for the presence of and expression of sulfur cycling genes. In these metagenomes, we found genes for sulfur reduction, oxidation and organic sulfur compound degradation. Metabolic pathway analysis showed presence of not only organic sulfur compounds contributing to the sulfur cycle, but tetrathionate, thiosulfate, and polysulfides playing a role as well. Using Lake Superior sediments, we also conducted sediment incubations to measure the biotransformation capability of sulfur-containing amino acids, sulfonates, and an analog for a common sulfolipid. Taurine and sodium dodecyl sulfate produced higher sulfate values in incubations, suggesting that microbes prefer sulfonates over sulfur-containing amino acids, in addition to a possible partiality towards oxidized organic sulfur compounds over reduced forms regarding sulfate production. The preference of sulfonates is supported by the commonality of taurine genes present as well as the low, but present transcription values of sulfoacetaldehyde degradation. While sulfur-containing amino acids do not produce sulfate values near that of sulfonates or sulfolipids, there are still present and transcriptionally active genes that can contribute to sulfate reduction in the system. Regarding methyl-sulfurs, metatranscriptomic data shows that methyl-mercaptan (intermediate within dimethyl sulfide and methionine degradation) degradation is transcriptionally active across genomes. By combining biotransformation incubation data, metagenomics, and metatranscriptomics, we analyzed how methylated sulfurs, sulfur-containing amino acids and sulfonates can fuel a sulfur cycle in a low-sulfate environment, informing us on how pathways may have operated in our Earth’s geologic past.