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Enterococcus faeciumis a commensal of the gastrointestinal tract of humans and animals. Since the 1990s, it has also emerged as a nosocomial pathogen. Little is known about carbon metabolism ofE. faeciumeven though the ability to utilize different sugars could be an important factor in adapting to different ecological niches. In this study we identify anE. faeciumgene cluster that is responsible for the metabolism of the α-galactoside sugar raffinose. Phenotypic testing of sevenE. faeciumisolates of which the genomes were previously sequenced showed that one isolate (strain E980) could grow on raffinose. Genome analysis identified a gene cluster containing two genes encoding α-galactosidases (termedagaAandagaB) that was uniquely present in E980. TheagaAandagaBgenes were significantly more frequently found in strains that are phylogenetically related to E980 and were more prevalent in surveillance isolates from hospital and community sources than in isolates from clinical infections. Disruption of the α-galactosidase geneagaB, but not ofagaA, disabled growth on raffinose in strain E980. In all strainsagaAandagaBare carried on megaplasmids that are between 150 and 300 kb in size. Filter-mating experiments showed that the megaplasmid of E980 can be transferred to a plasmidless recipient which then gains the ability to grow on raffinose. The observation that raffinose utilization byE. faeciumis a trait carried by megaplasmids indicates that these megaplasmids can have important roles in shaping the competitive fitness ofE. faeciumin the environment, for example by expanding the metabolic repertoire of this organism.