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 Bodelier; Wilbert Bitter

doi:10.1038/s41564-022-01252-3

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

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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 (US)
Journal	Nature Microbiology
DOIs	https://doi.org/10.1038/s41564-022-01252-3
State	Published - Nov 3 2022

Bibliographical note

KAUST Repository Item: Exported on 2022-11-07
Acknowledged KAUST grant number(s): BAS/1/1020-01-01
Acknowledgements: The authors thank C. Murrell for valuable discussions, C. P. Antony for assistance in metagenomics, A. Grootemaat for TEM imaging, M. Kienhuis for technical support with nanoSIMS analysis, I. Grigoriev for support during fluorescence microsopy, and Z. Para and B. Hegyeli, the Romanian custodians, for facilitating the experiments in Sulfur Cave. Also, we thank Utrecht Sequencing Facility (useq.nl) for providing sequencing service and data. The nanoSIMS facility at Utrecht University was financed through a large infrastructure grant by the Netherlands Organisation for Scientific Research (NWO, grant no. 175.010.2009.011). C.M. was supported by the Dutch Research Council, as part of the MiCRop Consortium (NWO/OCW grant no. 024.004.014). A.P. and Q.G. are supported by a faculty baseline grant (BAS/1/1020-01-01) from KAUST to A.P. The authors also thank members of the Bioscience Core Laboratory in KAUST for providing assistance with the generation of raw genome sequence datasets. PIE research was funded by FONDECYT-CONCYTEC (216-2015-FONDECYT). This is publication number 7467 of the Netherlands Institute of Ecology (NIOO-KNAW).

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van Spanning, R. J. M., Guan, Q., Melkonian, C., Gallant, J., Polerecky, L., Flot, J.-F., Brandt, B. W., Braster, M., Iturbe Espinoza, P., Aerts, J. W., Meima-Franke, M. M., Piersma, S. R., 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. 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}, {Rob J M} and Qingtian Guan and Chrats Melkonian and James Gallant and Lubos Polerecky and Jean-Fran{\c c}ois Flot and Brandt, {Bernd W} and Martin Braster and {Iturbe Espinoza}, Paul and Aerts, {Joost W} and Meima-Franke, {Marion M} and Piersma, {Sander R} 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 Bodelier, {Paul L E} and Wilbert Bitter",

note = "KAUST Repository Item: Exported on 2022-11-07 Acknowledged KAUST grant number(s): BAS/1/1020-01-01 Acknowledgements: The authors thank C. Murrell for valuable discussions, C. P. Antony for assistance in metagenomics, A. Grootemaat for TEM imaging, M. Kienhuis for technical support with nanoSIMS analysis, I. Grigoriev for support during fluorescence microsopy, and Z. Para and B. Hegyeli, the Romanian custodians, for facilitating the experiments in Sulfur Cave. Also, we thank Utrecht Sequencing Facility (useq.nl) for providing sequencing service and data. The nanoSIMS facility at Utrecht University was financed through a large infrastructure grant by the Netherlands Organisation for Scientific Research (NWO, grant no. 175.010.2009.011). C.M. was supported by the Dutch Research Council, as part of the MiCRop Consortium (NWO/OCW grant no. 024.004.014). A.P. and Q.G. are supported by a faculty baseline grant (BAS/1/1020-01-01) from KAUST to A.P. The authors also thank members of the Bioscience Core Laboratory in KAUST for providing assistance with the generation of raw genome sequence datasets. PIE research was funded by FONDECYT-CONCYTEC (216-2015-FONDECYT). This is publication number 7467 of the Netherlands Institute of Ecology (NIOO-KNAW).",

year = "2022",

month = nov,

day = "3",

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

language = "English (US)",

journal = "Nature Microbiology",

issn = "2058-5276",

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van Spanning, RJM, Guan, Q, Melkonian, C, Gallant, J, Polerecky, L, Flot, J-F, Brandt, BW, Braster, M, Iturbe Espinoza, P, Aerts, JW, Meima-Franke, MM, Piersma, SR, Bunduc, CM, Ummels, R, Pain, A, Fleming, EJ, van der Wel, NN, Gherman, VD, Sarbu, SM, Bodelier, PLE & Bitter, W 2022, 'Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem.', Nature Microbiology. 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, Rob J M

AU - Guan, Qingtian

AU - Melkonian, Chrats

AU - Gallant, James

AU - Polerecky, Lubos

AU - Flot, Jean-François

AU - Brandt, Bernd W

AU - Braster, Martin

AU - Iturbe Espinoza, Paul

AU - Aerts, Joost W

AU - Meima-Franke, Marion M

AU - Piersma, Sander R

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 L E

AU - Bitter, Wilbert

N1 - KAUST Repository Item: Exported on 2022-11-07 Acknowledged KAUST grant number(s): BAS/1/1020-01-01 Acknowledgements: The authors thank C. Murrell for valuable discussions, C. P. Antony for assistance in metagenomics, A. Grootemaat for TEM imaging, M. Kienhuis for technical support with nanoSIMS analysis, I. Grigoriev for support during fluorescence microsopy, and Z. Para and B. Hegyeli, the Romanian custodians, for facilitating the experiments in Sulfur Cave. Also, we thank Utrecht Sequencing Facility (useq.nl) for providing sequencing service and data. The nanoSIMS facility at Utrecht University was financed through a large infrastructure grant by the Netherlands Organisation for Scientific Research (NWO, grant no. 175.010.2009.011). C.M. was supported by the Dutch Research Council, as part of the MiCRop Consortium (NWO/OCW grant no. 024.004.014). A.P. and Q.G. are supported by a faculty baseline grant (BAS/1/1020-01-01) from KAUST to A.P. The authors also thank members of the Bioscience Core Laboratory in KAUST for providing assistance with the generation of raw genome sequence datasets. PIE research was funded by FONDECYT-CONCYTEC (216-2015-FONDECYT). This is publication number 7467 of the Netherlands Institute of Ecology (NIOO-KNAW).

PY - 2022/11/3

Y1 - 2022/11/3

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.

UR - http://hdl.handle.net/10754/685552

UR - https://www.nature.com/articles/s41564-022-01252-3

U2 - 10.1038/s41564-022-01252-3

DO - 10.1038/s41564-022-01252-3

M3 - Article

C2 - 36329197

SN - 2058-5276

JO - Nature Microbiology

JF - Nature Microbiology

ER -

Methanotrophy by a Mycobacterium species that dominates a cave microbial ecosystem.

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Bibliographical note

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