Non-thermodynamic factors affect competition between thermophilic chemolithoautotrophs from deep-sea hydrothermal...

Various environmental factors, including H₂ availability, metabolic tradeoffs, optimal growth temperature, stochasticity, and hydrology, were examined to determine if they affect microbial competition between three autotrophic thermophiles. The thiosulfate reducer Desulfurobacterium thermolithotrophum (T_opt72°C) was grown in mono- and coculture separately with the methanogens Methanocaldococcus jannaschii (T_opt82°C) at 72°C and Methanothermococcus thermolithotrophicus (T_opt65°C) at 65°C at high and low H₂ concentrations. Both methanogens showed a metabolic tradeoff shifting from high growth rate-low cell yield at high H₂ concentrations to low growth rate-high cell yield at low H₂ concentrations and when grown in coculture with the thiosulfate reducer. In 1:1 initial ratios, D. thermolithotrophum outcompeted both methanogens at high and low H₂, no H₂S was detected on low H₂, and it grew with only CO₂ as the electron acceptor indicating a similar metabolic tradeoff with low H₂. When the initial methanogen-to-thiosulfate reducer ratio varied from 1:1 to 10⁴:1 with high H₂, D. thermolithotrophum always outcompeted M. jannaschii at 72°C. However, M. thermolithotrophicus outcompeted D. thermolithotrophum at 65°C when the ratio was 10³:1. A reactive transport model that mixed pure hydrothermal fluid with cold seawater showed that hyperthermophilic methanogens dominated in systems where the residence time of the mixed fluid above 72°C was sufficiently high. With shorter residence times, thermophilic thiosulfate reducers dominated. If residence times increased with decreasing fluid temperature along the flow path, then thermophilic methanogens could dominate. Thermophilic methanogen dominance spread to previously thiosulfate-reducer-dominated conditions if the initial ratio of thermophilic methanogen-to-thiosulfate reducer increased.

The deep subsurface is the largest reservoir of microbial biomass on Earth and serves as an analog for life on the early Earth and extraterrestrial environments. Methanogenesis and sulfur reduction are among the more common chemolithoautotrophic metabolisms found in hot anoxic hydrothermal vent environments. Competition between H2-oxidizing sulfur reducers and methanogens is primarily driven by the thermodynamic favorability of redox reactions with the former outcompeting methanogens. This study demonstrated that competition between the hydrothermal vent chemolithoautotrophs Methanocaldococcus jannaschii, Methanothermococcus thermolithotrophicus, and Desulfurobacterium thermolithotrophum is also influenced by other overlapping factors such as staggered optimal growth temperatures, stochasticity, and hydrology. By modeling all aspects of microbial competition coupled with field data, a better understanding is gained on how methanogens can outcompete thiosulfate reducers in hot anoxic environments and how the deep subsurface contributes to biogeochemical cycling.