Physiological stress response to sulfide exposure of freshwater anaerobic methanotrophic archaea

Freshwater wetlands and coastal sediments are becoming hotspots for the emission of the greenhouse gas methane. Eutrophication-induced deposition of organic matter leads to elevated methanogenesis and sulfate reduction, thereby increasing the concentrations of methane and toxic sulfide, respectively. However, the effects of sulfide stress on the anaerobic methanotrophic biofilter have not been well explored. Here, we show how an enrichment culture dominated by the freshwater anaerobic methane-oxidizing archaeon Candidatus (Ca.) Methanoperedens responds to short-term and long-term exposure to sulfide in a bioreactor. The methane-oxidizing activity decreased to 45% and 20% but partially recovered to 70% and 30% within 5 days after short- and long-term sulfide exposure, respectively. Metagenomics indicated that Ca. Methanoperedens remained dominant in the enrichment throughout the entire experiment. The first short-term sulfide pulse led to increased expression of genes encoding for sulfide detoxification by low abundant community members, whereas long-term exposure resulted in upregulation of Ca. Methanoperedens genes encoding sulfite reductases of Group III (Dsr-LP). Ca. Methanoperedens consumed Polyhydroxyalkanoates during long-term sulfide exposure, possibly to aid in stress adaptation. Together, these results provide a valuable baseline for understanding fundamental ecophysiological adaptations in sulfate- and nitrate-rich aquatic ecosystems. Short synopsis statementThis study investigated how freshwater anaerobic methanotrophic archaea responded to sulfide exposure, revealing a transient inhibition and physiological adaptation mechanisms.