Physiological basis for atmospheric methane oxidation and methanotrophic growth on air

Tilman Schmider (), Anne Grethe Hestnes, Julia Brzykcy, Hannes Schmidt, Arno Schintlmeister, Benjamin R. K. Roller, Ezequiel Jesús Teran, Andrea Söllinger, Oliver Schmidt, Martin F. Polz, Andreas Richter, Mette M. Svenning and Alexander T. Tveit ()
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Tilman Schmider: UiT—The Arctic University of Norway
Anne Grethe Hestnes: UiT—The Arctic University of Norway
Julia Brzykcy: University of Warsaw
Hannes Schmidt: University of Vienna
Arno Schintlmeister: University of Vienna
Benjamin R. K. Roller: University of Vienna
Ezequiel Jesús Teran: Centro de Investigaciones en Física e Ingeniería del Centro de la Provincia de Buenos Aires (CIFICEN-UNCPBA-CONICET-CICPBA)
Andrea Söllinger: UiT—The Arctic University of Norway
Oliver Schmidt: UiT—The Arctic University of Norway
Martin F. Polz: University of Vienna
Andreas Richter: University of Vienna
Mette M. Svenning: UiT—The Arctic University of Norway
Alexander T. Tveit: UiT—The Arctic University of Norway

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Atmospheric methane oxidizing bacteria (atmMOB) constitute the sole biological sink for atmospheric methane. Still, the physiological basis allowing atmMOB to grow on air is not well understood. Here we assess the ability and strategies of seven methanotrophic species to grow with air as sole energy, carbon, and nitrogen source. Four species, including three outside the canonical atmMOB group USCα, enduringly oxidized atmospheric methane, carbon monoxide, and hydrogen during 12 months of growth on air. These four species exhibited distinct substrate preferences implying the existence of multiple metabolic strategies to grow on air. The estimated energy yields of the atmMOB were substantially lower than previously assumed necessary for cellular maintenance in atmMOB and other aerobic microorganisms. Moreover, the atmMOB also covered their nitrogen requirements from air. During growth on air, the atmMOB decreased investments in biosynthesis while increasing investments in trace gas oxidation. Furthermore, we confirm that a high apparent specific affinity for methane is a key characteristic of atmMOB. Our work shows that atmMOB grow on the trace concentrations of methane, carbon monoxide, and hydrogen present in air and outlines the metabolic strategies that enable atmMOB to mitigate greenhouse gases.

Date: 2024
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DOI: 10.1038/s41467-024-48197-1

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