Hydrogen-limited growth of hyperthermophilic methanogens at deep-sea hydrothermal vents

Abstract

Microbial productivity at hydrothermal vents is among the highest found anywhere in the deep ocean, but constraints on microbial growth and metabolism at vents are lacking. We used a combination of cultivation, molecular, and geochemical tools to verify pure culture H₂ threshold measurements for hyperthermophilic methanogenesis in low-temperature hydrothermal fluids from Axial Volcano and Endeavour Segment in the northeastern Pacific Ocean. Two Methanocaldococcus strains from Axial and Methanocaldococcus jannaschii showed similar Monod growth kinetics when grown in a bioreactor at varying H₂ concentrations. Their H₂ half-saturation value was 66 μM, and growth ceased below 17–23 μM H₂, 10-fold lower than previously predicted. By comparison, measured H₂ and CH₄ concentrations in fluids suggest that there was generally sufficient H₂ for Methanocaldococcus growth at Axial but not at Endeavour. Fluids from one vent at Axial (Marker 113) had anomalously high CH₄ concentrations and contained various thermal classes of methanogens based on cultivation and mcrA/mrtA analyses. At Endeavour, methanogens were largely undetectable in fluid samples based on cultivation and molecular screens, although abundances of hyperthermophilic heterotrophs were relatively high. Where present, Methanocaldococcus genes were the predominant mcrA/mrtA sequences recovered and comprised ∼0.2–6% of the total archaeal community. Field and coculture data suggest that H₂ limitation may be partly ameliorated by H₂ syntrophy with hyperthermophilic heterotrophs. These data support our estimated H₂ threshold for hyperthermophilic methanogenesis at vents and highlight the need for coupled laboratory and field measurements to constrain microbial distribution and biogeochemical impacts in the deep sea.