Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

R. Van Spanning* (Corresponding author), Q. Guan, Chrats Melkonian, James Gallant, Lubos Polerecky, Jean-François Flot, Bernd W Brandt, M. Braster, Paul Iturbe-Espinoza, Joost Aerts, M. Meima-Franke, S. Piersma, Catalin M. Bunduc, Roy Ummels, Arnab Pain, Emily J. Fleming, Nicole N. van der Wel, Vasile D. Gherman, Serban M. Sarbu, Paul BodelierW. Bitter

*Corresponding author for this work

Research output: Contribution to journal/periodicalArticleScientificpeer-review

Abstract

So far, only members of the bacterial phyla Proteobacteria and Verrucomicrobia are known to grow methanotrophically under aerobic conditions. Here we report that this metabolic trait is also observed within the Actinobacteria. We enriched and cultivated a methanotrophic Mycobacterium from an extremely acidic biofilm growing on a cave wall at a gaseous chemocline interface between volcanic gases and the Earth’s atmosphere. This Mycobacterium, for which we propose the name Candidatus Mycobacterium methanotrophicum, is closely related to well-known obligate pathogens such as M. tuberculosis and M. leprae. Genomic and proteomic analyses revealed that Candidatus M. methanotrophicum expresses a full suite of enzymes required for aerobic growth on methane, including a soluble methane monooxygenase that catalyses the hydroxylation of methane to methanol and enzymes involved in formaldehyde fixation via the ribulose monophosphate pathway. Growth experiments combined with stable isotope probing using 13C-labelled methane confirmed that Candidatus M. methanotrophicum can grow on methane as a sole carbon and energy source. A broader survey based on 16S metabarcoding suggests that species closely related to Candidatus M. methanotrophicum may be abundant in low-pH, high-methane environments.
Original languageEnglish
Pages (from-to)2089-2100
Number of pages12
JournalNature Microbiology
Volume7
Issue number12
Early online date2022
DOIs
Publication statusPublished - 2022

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