Desulfoluna spp. form a cosmopolitan group of anaerobic dehalogenating bacteria widely distributed in marine sponges

Abstract

Abstract Host-specific microbial communities thrive within sponge tissues and this association between sponge and associated microbiota may be driven by the organohalogen chemistry of the sponge animal. Several sponge species produce diverse organobromine secondary metabolites (e.g. brominated phenolics, indoles, and pyrroles) that may function as a chemical defense against microbial fouling, infection or predation. In this study, anaerobic cultures prepared from marine sponges were amended with 2,6-dibromophenol as the electron acceptor and short chain organic acids as electron donors. We observed reductive dehalogenation from diverse sponge species collected at disparate temperate and tropical waters suggesting that biogenic organohalides appear to enrich for populations of dehalogenating microorganisms in the sponge animal. Further enrichment by successive transfers with 2,6-dibromophenol as the sole electron acceptor demonstrated the presence of dehalogenating bacteria in over 20 sponge species collected from temperate and tropical ecoregions in the Atlantic and Pacific Oceans and the Mediterranean Sea. The enriched dehalogenating strains were closely related to Desulfoluna spongiiphila and Desulfoluna butyratoxydans, suggesting a cosmopolitan association between Desulfoluna spp. and various marine sponges. In vivo reductive dehalogenation in intact sponges was also demonstrated. Organobromide-rich sponges may thus provide a specialized habitat for organohalide-respiring microbes and D. spongiiphila and/or its close relatives are responsible for reductive dehalogenation in geographically widely distributed sponge species.