An uncharacterized clade in the DMSO reductase family of molybdenum oxidoreductases is a new type of chlorate reductase.

ABSTRACT

The dimethylsulfoxide (DMSO) reductase family of enzymes has many subfamilies catalysing unique biogeochemical reactions. It also has many uncharacterized subfamilies. Comparative genomics predicted one such subfamily to participate in a key step of the chlorine cycle because of a conserved genetic association with chlorite dismutase, implying they produce chlorite through chlorate or perchlorate reduction. We determined the activity of the uncharacterized enzyme by comparing strains in the phototrophic genus Rhodoplanes that encode either a typical perchlorate reductase or the uncharacterized enzyme. Rpl. piscinae and Rpl. elegans, which encode perchlorate reductase, grew by using perchlorate as an electron acceptor. In contrast, Rpl. roseus, which encodes the uncharacterized enzyme, grew by chlorate reduction but not by perchlorate reduction. This is the first report of perchlorate and chlorate being used as respiratory electron acceptors by phototrophs. When both chlorate and perchlorate were present, Rpl. roseus consumed only chlorate. Highly concentrated Rpl. roseus cells showed some perchlorate consumption, but chlorate consumption occurred at a 10-fold higher rate. Together, these genomic and physiological data define a new group of chlorate reductases. Some organisms encode both this chlorate reductase and a perchlorate reductase, raising new questions about the physiology and evolution of chlorine oxyanion respiration.