Exploring Volatile Sulfur Production by Arctic Soil Bacteria and Emissions from Thawing Permafrost

Warming of the Arctic enhances microbial activity and the decomposition of large stocks of organic matter retained in permafrost soil. Resulting changes in the availability of sulfur may lead to increased emissions of volatile sulfur compounds (VSCs), which impact atmospheric particle and cloud formation, terrestrial and aquatic acidification, and malodor. Marine microbial production of dimethyl sulfide (DMS) has been studied for decades but other VSCs have been largely ignored, while VSC emissions from terrestrial ecosystems are even less studied. Currently, we lack fundamental understanding of the metabolic processes behind VSC production in permafrost soil bacteria, essential for estimating how emissions may change due to thawing. To fill this knowledge gap, we measured VSC emissions from thawing permafrost and three bacterial strains isolated from Greenlandic permafrost and biological soil crust. We show that the bacterial strains produced high levels of VSCs in vitro - including hydrogen sulfide, methanethiol, DMS, dimethyl disulfide, and dimethyl trisulfide. We further show that the same VSCs were also emitted from permafrost upon thaw. Metabolic pathway mapping of the bacterial strains revealed both inorganic sulfate reduction pathways and amino acid metabolism behind bacterial VSC production. High production of VSCs in the late-active and stationary phase suggests connection to secondary metabolism, except for DMS which was linked to early growth, and possibly, primary energy metabolism. Our findings suggest that thawing increases VSC emissions from permafrost soil, possibly leading to higher input of sulfur into the atmosphere from the warming Arctic in the future.