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Hyperthermophilic methanogens are often H 2 limited in hot subseafloor environments, and their survival may be due in part to physiological adaptations to low H 2 conditions and interspecies H 2 transfer. The hyperthermophilic methanogen Methanocaldococcus jannaschii was grown in monoculture at high (80 to 83 μM) and low (15 to 27 μM) aqueous H 2 concentrations and in coculture with the hyperthermophilic H 2 producer Thermococcus paralvinellae The purpose was to measure changes in growth and CH 4 production kinetics, CH 4 fractionation, and gene expression in M. jannaschii with changes in H 2 flux. Growth and cell-specific CH 4 production rates of M. jannaschii decreased with decreasing H 2 availability and decreased further in coculture. However, cell yield (cells produced per mole of CH 4 produced) increased 6-fold when M. jannaschii was grown in coculture rather than monoculture. Relative to high H 2 concentrations, isotopic fractionation of CO 2 to CH 4 (ε CO2-CH4 ) was 16‰ larger for cultures grown at low H 2 concentrations and 45‰ and 56‰ larger for M. jannaschii growth in coculture on maltose and formate, respectively. Gene expression analyses showed H 2 -dependent methylene-tetrahydromethanopterin (H 4 MPT) dehydrogenase expression decreased and coenzyme F 420 -dependent methylene-H 4 MPT dehydrogenase expression increased with decreasing H 2 availability and in coculture growth. In coculture, gene expression decreased for membrane-bound ATP synthase and hydrogenase. The results suggest that H 2 availability significantly affects the CH 4 and biomass production and CH 4 fractionation by hyperthermophilic methanogens in their native habitats. IMPORTANCE Hyperthermophilic methanogens and H 2 -producing heterotrophs are collocated in high-temperature subseafloor environments, such as petroleum reservoirs, mid-ocean ridge flanks, and hydrothermal vents. Abiotic flux of H 2 can be very low in these environments, and there is a gap in our knowledge about the origin of CH 4 in these habitats. In the hyperthermophile Methanocaldococcus jannaschii , growth yields increased as H 2 flux, growth rates, and CH 4 production rates decreased. The same trend was observed increasingly with interspecies H 2 transfer between M. jannaschii and the hyperthermophilic H 2 producer Thermococcus paralvinellae With decreasing H 2 availability, isotopic fractionation of carbon during methanogenesis increased, resulting in isotopically more negative CH 4 with a concomitant decrease in H 2 -dependent methylene-tetrahydromethanopterin dehydrogenase gene expression and increase in F 420 -dependent methylene-tetrahydromethanopterin dehydrogenase gene expression. The significance of our research is in understanding the nature of hyperthermophilic interspecies H 2 transfer and identifying biogeochemical and molecular markers for assessing the physiological state of methanogens and possible source of CH 4 in natural environments.

applied and environmental microbiology

Growth Kinetics, Carbon Isotope Fractionation, and Gene Expression in the Hyperthermophile <i>Methanocaldococcus jannaschii</i> during Hydrogen-Limited Growth and Interspecies Hydrogen Transfer

Growth Kinetics, Carbon Isotope Fractionation, and Gene Expression in the Hyperthermophile Methanocaldococcus jannaschii during Hydrogen-Limited Growth and Interspecies Hydrogen Transfer