Microbial cysteine degradation is a source of hydrogen sulfide in oxic freshwater lakes

Abstract

AbstractThe sulfur-containing amino acid cysteine is abundant in the environment including in freshwater lakes. Biological degradation of cysteine can result in hydrogen sulfide (H2S), a toxic and ecologically relevant compound that is a central player in biogeochemical cycling in aquatic environments, including freshwater lakes. Here, we investigated the ecological significance of cysteine in oxic freshwater lake environments, using model systems of isolated cultures, controlled growth experiments, and multi-omics. We screened bacterial isolates enriched from natural lake water for their ability to produce H2S when provided cysteine. In total, we identified 29 isolates that produced H2S and belonged to the phylum proteobacteria Bacteroidetes, Proteobacteria and Actinobacteria. To understand the genomic and genetic basis for cysteine degradation and H2S production, we further characterized 3 freshwater isolates using whole-genome sequencing, and quantitatively tracked cysteine and H2S levels over their growth ranges: Stenotrophomonas maltophila, Stenotrophomonas bentonitica (Gammaproteobacteria) and Chryseobacterium piscium (Bacteroidetes). We observed a decrease in cysteine and increase in H2S, and identified genes involved in cysteine degradation in all 3 genomes. Finally, to assess the presence of these organisms and genes in the environment, we surveyed a five-year time series of metagenomic data from the same isolation source at Lake Mendota and identified their presence throughout the time series. Overall, our study shows that sulfur-containing amino acids can drive microbial H2S production in oxic environments. Future considerations of sulfur cycling and biogeochemistry in oxic environments should account for H2S production from degradation of organosulfur compounds.ImportanceHydrogen sulfide (H2S), a naturally occurring gas with biological origins, can be toxic to living organisms. In aquatic environments, H2S production typically originates from anoxic (lacking oxygen) environments such as sediments, or the bottom layers of lakes. However, the degradation of sulfur-containing amino acids such as cysteine, which all cells and life forms rely on, can be a source of ammonia and H2S in the environment. Unlike other approaches for the biological production of H2S such as dissimilatory sulfate reduction, cysteine degradation can occur in the presence of oxygen. Yet, little is known about how cysteine degradation influences sulfur availability and cycling in freshwater lakes. In our study, we found that multiple bacteria originating from a freshwater lake can not only produce H2S, but do so in oxic conditions. Overall, our study highlights the ecological importance of oxic H2S production in natural ecosystems, and necessitates a change in our outlook of sulfur biogeochemistry.