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The bacterial Wood-Ljungdahl pathway for CO2-reductive acetogenesis is important for the nutritional mutualism occurring between wood-feeding insects and their hindgut microbiota. A key step in this pathway is the reduction of CO2 to formate, catalysed by the enzyme formate dehydrogenase (FDH). Putative selenocysteine- (Sec) and cysteine- (Cys) containing paralogues of hydrogenase-linked FDH (FDHH) have been identified in the termite gut acetogenic spirochete,Treponema primitia, but knowledge of their relevance in the termite gut environment remains limited. In this study, we designed degenerate PCR primers for FDHH genes (fdhF) and assessedfdhFdiversity in insect gut bacterial isolates and the gut microbial communities of termites and cockroaches. The insects examined herein represent three wood-feeding termite families,Termopsidae,KalotermitidaeandRhinotermitidae(phylogenetically ‘lower’ termite taxa); the wood-feeding roach familyCryptocercidae(the sister taxon to termites); and the omnivorous roach familyBlattidae. Sec and Cys FDHH variants were identified in every wood-feeding insect but not the omnivorous roach. Of 68 novel alleles obtained from inventories, 66 affiliated phylogenetically with enzymes fromT. primitia. These formed two subclades (37 and 29 phylotypes) almost completely comprised of Sec-containing and Cys-containing enzymes respectively. A gut cDNA inventory showed transcription of both variants in the termiteZootermopsis nevadensis(familyTermopsidae). The gene patterns suggest that FDHH enzymes are important for the CO2-reductive metabolism of uncultured acetogenic treponemes and imply that the availability of selenium, a trace element, shaped microbial gene content in the last common ancestor of dictyopteran, wood-feeding insects, and continues to shape it to this day.