Extremeophiles and Extreme Environments

Non-thermodynamic Factors Affect Competition Between Thermophilic Chemolithoautotrophs From Deep-sea Hydrothermal Vents

By Keith Cowing
Status Report
Appl Environ Microbiol via PubMed
September 25, 2024
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Non-thermodynamic Factors Affect Competition Between Thermophilic Chemolithoautotrophs From Deep-sea Hydrothermal Vents
Reactive transport modeling results for (A) pipe-like (high xb) and (B) plume-like (low xb) fluid flow. The heat maps (C–F) show the predominant thermophile (M. jannaschii in red, D. thermolithotrophum in yellow, and M. thermolithotrophicus in blue) at varying xb values and subseafloor residence times below 85°C. H2 concentrations in and temperature of pure hydrothermal vent fluids were 300 µM and 214°C (C, D) and 950 µM and 330°C (E, F) representing Marker 33 and Marker 113, respectively, at Axial Seamount. The initial M. jannaschii:D. thermolithotrophum:M. thermolithotrophicus ratios were either 1:1:1 (C, E) or 1:1:100 (D, F). The conditions that best fit the field results for Marker 33 and Marker 113 are indicated with an F symbol in the heat map. via PubMed

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 (Topt72°C) was grown in mono- and coculture separately with the methanogens Methanocaldococcus jannaschii (Topt82°C) at 72°C and Methanothermococcus thermolithotrophicus (Topt65°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.

Non-thermodynamic factors affect competition between thermophilic chemolithoautotrophs from deep-sea hydrothermal vents, Appl Environ Microbiol v.90(8); 2024 Aug PMC11337833 (open access) via PubMed

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