The massive global release of halogenated hydrocarbons (organohalides) over the last century caused severe detrimental effects on human and environmental health. Research on the biological degradation of organohalides revealed the discovery of several bacteria able to dehalogenate and thus detoxify these pollutants by utilizing them as terminal electron acceptors in organohalide respiration. The organohalide-respiring -proteobacterium Sulfurospirillum multivorans was extensively studied for its tetrachloroethene (PCE) reductive dehalogenase PceA and has become a model organism for organohalide respiration. However, the hydrogen metabolism which might be involved in the respiratory chain and possible syntrophic interactions of this organism with bacteria in its natural habitat has never been characterized and are the focus of this study. Four [NiFe] hydrogenases have been identified in the genome, of which one membrane-bound H2-oxidizing (MBH) and one H2-producing (Hyf) enzyme were found to be expressed. Biochemical characterization of a MBH-enrichment implicate the enzyme as possible electron donating system of the organohalide respiratory chain. The other hydrogenase was transcribed during pyruvate fermentation and screening of different Sulfurospirillum spp. revealed a fermentative hydrogen production of these bacteria for the first time. Fermentation balances and comparative proteomics were performed to elucidate the metabolic pathways of pyruvate fermentation and a remarkable upregulation of the Hyf hydrogenase and other pyruvate-metabolizing enzymes was observed. Co-cultivation of S. multivorans with another organohalide-respiring bacterium, Dehalococcoides mccartyi, introduced the organism as a H2-producing syntrophic partner and uncovered a new ecological role. An interspecies hydrogen and cobamide transfer enabled a fast and complete dechlorination of the prominent groundwater pollutant PCE to ethene which is of high interest for bioremediation processes.