Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

R. Van Spanning; 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 Bodelier; W. Bitter

doi:10.1038/s41564-022-01252-3

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

NIOO - Microbial Ecology (ME)

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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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 language	English
Pages (from-to)	2089-2100
Number of pages	12
Journal	Nature Microbiology
Volume	7
Issue number	12
Early online date	2022
DOIs	https://doi.org/10.1038/s41564-022-01252-3
Publication status	Published - 2022

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Van Spanning, R., Guan, Q., Melkonian, C., Gallant, J., Polerecky, L., Flot, J.-F., Brandt, B. W., Braster, M., Iturbe-Espinoza, P., Aerts, J., Meima-Franke, M., Piersma, S., Bunduc, C. M., Ummels, R., Pain, A., Fleming, E. J., van der Wel, N. N., Gherman, V. D., Sarbu, S. M., ... Bitter, W. (2022). Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem. Nature Microbiology, 7(12), 2089-2100. https://doi.org/10.1038/s41564-022-01252-3

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title = "Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem",

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{\textquoteright}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.",

author = "{Van Spanning}, R. and Q. Guan and Chrats Melkonian and James Gallant and Lubos Polerecky and Jean-Fran{\c c}ois Flot and Brandt, {Bernd W} and M. Braster and Paul Iturbe-Espinoza and Joost Aerts and M. Meima-Franke and S. Piersma and Bunduc, {Catalin M.} and Roy Ummels and Arnab Pain and Fleming, {Emily J.} and {van der Wel}, {Nicole N.} and Gherman, {Vasile D.} and Sarbu, {Serban M.} and Paul Bodelier and W. Bitter",

note = "7465, ME; Data archiving: no NIOO data",

year = "2022",

doi = "10.1038/s41564-022-01252-3",

language = "English",

volume = "7",

pages = "2089--2100",

journal = "Nature Microbiology",

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Van Spanning, R, Guan, Q, Melkonian, C, Gallant, J, Polerecky, L, Flot, J-F, Brandt, BW, Braster, M, Iturbe-Espinoza, P, Aerts, J, Meima-Franke, M, Piersma, S, Bunduc, CM, Ummels, R, Pain, A, Fleming, EJ, van der Wel, NN, Gherman, VD, Sarbu, SM, Bodelier, P & Bitter, W 2022, 'Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem', Nature Microbiology, vol. 7, no. 12, pp. 2089-2100. https://doi.org/10.1038/s41564-022-01252-3

TY - JOUR

T1 - Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

AU - Van Spanning, R.

AU - Guan, Q.

AU - Melkonian, Chrats

AU - Gallant, James

AU - Polerecky, Lubos

AU - Flot, Jean-François

AU - Brandt, Bernd W

AU - Braster, M.

AU - Iturbe-Espinoza, Paul

AU - Aerts, Joost

AU - Meima-Franke, M.

AU - Piersma, S.

AU - Bunduc, Catalin M.

AU - Ummels, Roy

AU - Pain, Arnab

AU - Fleming, Emily J.

AU - van der Wel, Nicole N.

AU - Gherman, Vasile D.

AU - Sarbu, Serban M.

AU - Bodelier, Paul

AU - Bitter, W.

N1 - 7465, ME; Data archiving: no NIOO data

PY - 2022

Y1 - 2022

N2 - 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.

AB - 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.

U2 - 10.1038/s41564-022-01252-3

DO - 10.1038/s41564-022-01252-3

M3 - Article

SN - 2058-5276

VL - 7

SP - 2089

EP - 2100

JO - Nature Microbiology

JF - Nature Microbiology

IS - 12

ER -

Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem

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