Dehalogenating Chloroflexi, such as Dehalococcoides (Dhc) strains, are members of the rare biosphere and were originally discovered as the key microbes mediating reductive dehalogenation of the prevalent groundwater contaminants tetrachloroethene (PCE) and trichloroethene (TCE) to ethene. Molecular and our genomic studies on the key enzymes, reductive dehalogenase encoded by rdh genes, have provided evidence for the rapid adaptive evolution of Dhc and rdh. Dehalococcoides are slow growing, highly niche adapted, strictly anaerobic microbes, that depend on a supporting microbial community for electron donor and cofactor requirements among other factors. Besides these interesting metabolic interactions, the more profound question though is: what is the metabolic life style of Dhc in the absence of anthropogenic contaminants? The genomic analysis of single cells obtained in this work from deep-‐sea sediments of the Peruvian Margin clearly revealed that these Chloroflexiare related to terrestrial reductively dehalogenating Dehaloccodia, yet carry no reductive dehalogenases, and instead have a lifestyle as homoacetogenic bacteria. Interestingly and importantly, we discovered a gene encoding a formate dehydrogenase (FdnI) with reciprocal closest identity to the formate dehydrogenase-‐like protein (complex iron sulfur molybdoenzyme, CISM) of terrestrialDehalococcoides/Dehalogenimonas spp. This finding of a close functional homolog provides an important missing link for understanding the origin and the metabolic core of terrestrial Dehalococcoides/Dehalogenimonas spp. and of reductive dehalogenation, as well as the biology of abundant deep-‐sea Chloroflexi.