Formate and hydrogen in hydrothermal vents and their use by extremely thermophilic methanogens and heterotrophs

Extremely thermophilic methanogens in the Methanococci and heterotrophs in the Thermococci are common in deep-sea hydrothermal vents. All Methanococci use H-2 as an electron donor, and a few species can also use formate. Most Methanococci have a coenzyme F-420-reducing formate dehydrogenase. All Thermococci reduce S-0 but have hydrogenases and produce H-2 in the absence of S-0. Some Thermococci have formate hydrogenlyase (Fhl) that reversibly converts H-2 and CO2 to formate or an NAD(P)(+)-reducing formate dehydrogenase (Nfd). Questions remain if Methanococci or Thermococci use or produce formate in nature, why only certain species can grow on or produce formate, and what the physiological role of formate is? Formate forms abiotically in hydrothermal fluids through chemical equilibrium with primarily H-2, CO2, and CO and is strongly dependent upon H-2 concentration, pH, and temperature. Formate concentrations are highest in hydrothermal fluids where H-2 concentrations are also high, such as in ultramafic systems where serpentinization reactions occur. In nature, Methanococci are likely to use formate as an electron donor when H-2 is limiting. Thermococci with Fhl likely convert H-2 and CO2 to formate when H-2 concentrations become inhibitory for growth. They are unlikely to grow on formate in nature unless formate is more abundant than H-2 in the environment. Nearly all Methanococci and Thermococci have a gene for at least one formate dehydrogenase catalytic subunit, which may be used to provide free formate for de novo purine biosynthesis. However, only species with a membrane-bound formate transporter can grow on or secrete formate. Interspecies H-2 transfer occurs between Thermococci and Methanococci. This and putative interspecies formate transfer may support Methanococci in low H-2 environments, which in turn may prevent growth inhibition of Thermococci by its own H-2. Future research directions include understanding when, where, and how formate is used and produced by these organisms in nature, and how transcription of Thermococci genes encoding formate-related enzymes are regulated.