Formate-driven growth coupled with H-2 production

Abstract

Although a common reaction in anaerobic environments, the conversion of formate and water to bicarbonate and H-2 (with a change in Gibbs free energy of Delta G degrees = + 1.3 kJ mol(-1)) has not been considered energetic enough to support growth of microorganisms. Recently, experimental evidence for growth on formate was reported for syntrophic communities of Moorella sp. strain AMP and a hydrogen-consuming Methanothermobacter species and of Desulfovibrio sp. strain G11 and Methanobrevibacter arboriphilus strain AZ(1). The basis of the sustainable growth of the formate-users is explained by H-2 consumption by the methanogens, which lowers the H-2 partial pressure, thus making the pathway exergonic(2). However, it has not been shown that a single strain can grow on formate by catalysing its conversion to bicarbonate and H-2. Here we report that several hyperthermophilic archaea belonging to the Thermococcus genus are capable of formate-oxidizing, H-2-producing growth. The actual Delta G values for the formate metabolism are calculated to range between -8 and -20 kJ mol(-1) under the physiological conditions where Thermococcus onnurineus strain NA1 are grown. Furthermore, we detected ATP synthesis in the presence of formate as a sole energy source. Gene expression profiling and disruption identified the gene cluster encoding formate hydrogen lyase, cation/proton antiporter and formate transporter, which were responsible for the growth of T. onnurineus NA1 on formate. This work shows formate-driven growth by a single microorganism with protons as the electron acceptor, and reports the biochemical basis of this ability.