Simultaneous sulfide and methane oxidation by an extremophile

Abstract

Hydrogen sulfide (H₂S) and methane (CH₄) are produced in anoxic environments through sulfate reduction and organic matter decomposition. Both gases diffuse upwards into oxic zones where aerobic methanotrophs mitigate CH₄ emissions by oxidizing this potent greenhouse gas. Although methanotrophs in myriad environments encounter toxic H₂S, it is virtually unknown how they are affected. Here, through extensive chemostat culturing we show that a single microorganism can oxidize CH₄ and H₂S simultaneously at equally high rates. By oxidizing H₂S to elemental sulfur, the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV alleviates the inhibitory effects of H₂S on methanotrophy. Strain SolV adapts to increasing H₂S by expressing a sulfide-insensitive ba₃-type terminal oxidase and grows as chemolithoautotroph using H₂S as sole energy source. Genomic surveys revealed putative sulfide-oxidizing enzymes in numerous methanotrophs, suggesting that H₂S oxidation is much more widespread in methanotrophs than previously assumed, enabling them to connect carbon and sulfur cycles in novel ways.

Fig. 1. Growth of M. fumariolicum SolV at high loads of CH₄ only, H₂S and CH₄, or H₂S only.

a Continuous culture oxidizing methane. b Continuous culture simultaneously oxidizing high concentrations of CH₄ and H₂S. c Fed-batch culture showing increase in ¹³C-biomass with H₂S as sole energy source. Data are presented as mean ± standard deviations (n = 3 technical replicates). Source data are provided as a Source Data file.

Fig. 2. Inhibition of CH₄ consumption by non-adapted Methylacidiphilum fumariolicum SolV cells in the presence of H₂S.

H₂S was kept at various stable concentrations (indicated at the bottom) by pulse-wise additions of H₂S to the MIMS chamber. Numbers indicate CH₄ consumption rates in μmol CH₄ · min⁻¹ · g DW⁻¹. At 170 min the MIMS chamber has become anoxic, resulting in cessation of CH₄ consumption. Source data are provided as a Source Data file.

Fig. 3. Inhibition of H₂S consumption by Methylacidiphilum fumariolicum SolV cells in the presence of methanol.

a Cessation of H₂S consumption by non-adapted cells after the addition of methanol (final concentration 0.4 mM). b Inhibition of H₂S consumption by sulfide-adapted cells after the addition of methanol (final concentration 5 mM). Numbers indicate consumption rates in μmol H₂S · min⁻¹ · g DW⁻¹. The black horizontal line indicates a brief moment of anoxia to demonstrate H₂S oxidation is dependent on O₂. Source data are provided as a Source Data file.

Fig. 4. H₂ and H₂S consumption dynamics in non-adapted Methylacidiphilum fumariolicum SolV cells.

Green numbers indicate H₂ consumption rates in μmol · min⁻¹ · g DW⁻¹ before and after H₂S addition, respectively. The red number and line indicate H₂S consumption rate in μmol · min⁻¹ · g DW⁻¹ after depletion of H₂. Source data are provided as a Source Data file.

Fig. 5. Kinetics of H₂S oxidation by Methylacidiphilum fumariolicum SolV cells.

a H₂S oxidation measured through gas chromatography. Different blue shaded diamonds represent biological replicates (n = 3). The reaction was initiated by addition of cells after 33 min. b H₂S respiration measured through a fiber-optic oxygen sensor spot in the MIMS chamber. Black lines indicate Michaelis-Menten curve fitting. The reaction was initiated by addition of cells at 0 min. Source data are provided as a Source Data file.