Halo(natrono)archaea from hypersaline lakes can utilize sulfoxides other than DMSO as electron acceptors for anaerobic respiration

Abstract

Dimethylsulfoxide (DMSO) has long been known to support anaerobic respiration in a few species of basically aerobic extremely halophilic euryarchaea living in hypersaline lakes. Recently, it has also been shown to be utilized as an additional electron acceptor in basically anaerobic sulfur-reducing haloarchaea. Here we investigated whether haloarchaea would be capable of anaerobic respiration with other two sulfoxides, methionine sulfoxide (MSO) and tetramethylene sulfoxide (TMSO). For this, anaerobic enrichment cultures were inoculated with sediments from hypersaline salt and soda lakes in southwestern Siberia and southern Russia. Positive enrichments were obtained for both MSO and TMSO with yeast extract but not with formate or acetate as the electron donor. Two pure cultures obtained from salt lakes, either with MSO or TMSO, were obligate anaerobes closely related to sulfur-reducing Halanaeroarchaeum sulfurireducens, although the type strain of this genus was unable to utilize any sulfoxides. Two pure cultures isolated from soda lakes were facultatively anaerobic alkaliphilic haloarchaea using O₂, sulfur and sulfoxides as the electron acceptors. One isolate was identical to the previously described sulfur-reducing Natrarchaeobaculum sulfurireducens, while another one, enriched at lower alkalinity, is forming a new species in the genus Halobiforma. Since all isolates enriched with either MSO or TMSO were able to respire all three sulfoxides including DMSO and the corresponding activities were cross-induced, it suggest that a single enzyme of the DMSO-reductase family with a broad substrate specificity is responsible for various sulfoxide-dependent respiration in haloarchaea.

Keywords: Anaerobic respiration; Haloarchaea; Hypersaline lakes; Methionine sulfoxide; Tetramethylene sulfoxide.