Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

Rob J.M. van Spanning*, Qingtian Guan, Chrats Melkonian, James Gallant, Lubos Polerecky, Jean François Flot, Bernd W. Brandt, Martin Braster, Paul Iturbe Espinoza, Joost W. Aerts, Marion M. Meima-Franke, Sander R. Piersma, Catalin M. Bunduc, Roy Ummels, Arnab Pain, Emily J. Fleming, Nicole N. van der Wel, Vasile D. Gherman, Serban M. Sarbu, Paul L.E. BodelierWilbert Bitter

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

29 Citations (Scopus)

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
JournalNature Microbiology
Volume7
DOIs
Publication statusPublished - 3 Nov 2022
Externally publishedYes

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