Termite hindguts are populated by a dense and diverse community of microbial symbionts working in concert to transform lignocellulosic plant material and derived residues into acetate, to recycle and fix nitrogen, and to remove oxygen. Although much has been learned about the breadth of microbial diversity in the hindgut, the ecophysiological roles of its members is less understood. In this study, we present new information about the ecophysiology of microorganism Diplosphaera colotermitum strain TAV2, an autochthonous member of the Reticulitermes flavipes gut community. An integrated high-throughput approach was used to determine the transcriptomic and proteomic profiles of cells grown under hypoxia (2% O2) or atmospheric (20% O2) concentrations of oxygen. Our results revealed that genes and proteins associated with energy production and utilization, carbohydrate transport and metabolism, nitrogen fixation, and replication and recombination were upregulated under 2% O2. The metabolic map developed for TAV2 indicates that this microorganism may be involved in biological nitrogen fixation, amino-acid production, hemicellulose degradation and consumption of O2 in the termite hindgut. Variation of O2 concentration explained 55.9% of the variance in proteomic profiles, suggesting an adaptive evolution of TAV2 to the hypoxic periphery of the hindgut. Our findings advance the current understanding of microaerophilic microorganisms in the termite gut and expand our understanding of the ecological roles for members of the phylum Verrucomicrobia.