Dimethyl sulfoxide reduction by a hyperhermophilic archaeon Thermococcus onnurineus NA1 via a cysteine-cystine redox shuttle

Abstract

To date, a variety of microbes are known to grow by respiration with dimethyl sulfoxide (DMSO) as an electron acceptor, and several distinct DMSO respiratory systems, consisting of electron carriers and a terminal DMSO reductase, have been characterized, especially intensively in Escherichia coli and Rhodopseudomonas capsula. In the course of investigating the growth of a hyperthermophilic archaeon Thermococcus onnurineus NA1, we observed that growth on peptides was also enhanced by the addition of DMSO. Attempts were made to measure the DMSO reductase activity and purify the DMSO reductase from cells, but cell extracts exhibited no DMSO-reducing activity. In search of a factor to confer on cells the ability of reducing DMSO, we found significant DMSO reduction by the addition of cystine in the cell extracts. In this study, we presented a novel mechanism for DMSO reduction. The archaeon reduced DMSO via a cysteine-cystine redox shuttle through a mechanism whereby cystine is microbially reduced to cysteine, which is then reoxidized by DMSO reduction. If cysteine-cystine shuttle acts as an electron carrier, microbes must have a system to regenerate cysteine by reducing cystine. A thioredoxin reductase-protein disulfide oxidoreductase redox couple was identified to have intracellular cystine-reducing activity. This study presents the first example of DMSO reduction via an electron shuttle. The members of the order Thermcharacterized, especially intensively in Escherichia coli and Rhodopseudomonas capsula. In the course of investigating the growth of a hyperthermophilic archaeon Thermococcus onnurineus NA1, we observed that growth on peptides was also enhanced by the addition of DMSO. Attempts were made to measure the DMSO reductase activity and purify the DMSO reductase from cells, but cell extracts exhibited no DMSO-reducing activity. In search of a factor to confer on cells the ability of reducing DMSO, we found significant DMSO reduction by the addition of cystine in the cell extracts. In this study, we presented a novel mechanism for DMSO reduction. The archaeon reduced DMSO via a cysteine-cystine redox shuttle through a mechanism whereby cystine is microbially reduced to cysteine, which is then reoxidized by DMSO reduction. If cysteine-cystine shuttle acts as an electron carrier, microbes must have a system to regenerate cysteine by reducing cystine. A thioredoxin reductase-protein disulfide oxidoreductase redox couple was identified to have intracellular cystine-reducing activity. This study presents the first example of DMSO reduction via an electron shuttle. The members of the order Therm