An obligately aerobic soil bacterium activates fermentative hydrogen production to survive reductive stress during hypoxia
Open accessAbstract
Significance: Obligate aerobes require survival strategies to persist in temporarily oxygen-deprived environments. In this article, we reveal a previously unidentified survival mechanism for obligately aerobic bacteria. Under oxygen-limiting conditions, the saprophytic actinomycete Mycobacterium smegmatis can rapidly switch between fermentative hydrogen production and hydrogen oxidation coupled to either oxygen or fumarate reduction depending on electron acceptor availability. To our knowledge, these results demonstrate for the first time (i) hydrogen production in an obligate aerobe, (ii) the unambiguous confirmation of fermentation in a mycobacterium and (iii) strong evidence that hydrogen has a role in survival and not just growth.
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Mycobacteria encode multiple flavin/deazaflavin oxidoreductases and hydride transferases to survive these stresses.
“encode multiple flavin/deazaflavin oxidoreductases and hydride transferases to survive these stresses (171–174)”
From Mycobacterium smegmatis: The Vanguard of Mycobacterial Research (2023) · cites this paper as [171]
The Significance section (page unavailable) identifies three [NiFe]-hydrogenases in M. smegmatis, and the Hydrogen Cycling Maintains Intracellular Redox Homeostasis section links Hyd2 and Hyd3 to maintaining redox balance during oxygen limitation. The paper does not identify these enzymes as multiple flavin/deazaflavin oxidoreductases or hydride transferases; it only describes a predicted FAD-binding motif in Hyd3. (LLM, conf=0.76)
Experimental — accuracy not yet measuredMycobacteria can metabolize hydrogen gas.
“Studies using the M. smegmatis toolbox have shown that mycobacteria can metabolize hydrogen gas, detoxify carbon monoxide, and encode multiple flavin/deazaflavin oxidoreductases and hydride transferases to survive these stresses (171–174).”
From Mycobacterium smegmatis: The Vanguard of Mycobacterial Research (2023) · cites this paper as [171]
Mycobacteria can detoxify carbon monoxide.
“mycobacteria can metabolize hydrogen gas, detoxify carbon monoxide, and encode multiple flavin/deazaflavin oxidoreductases and hydride transferases to survive these stresses (171–174)”
From Mycobacterium smegmatis: The Vanguard of Mycobacterial Research (2023) · cites this paper as [171]
The Significance and hydrogenase results describe hydrogen production, oxidation, and survival during hypoxia, but do not address carbon monoxide detoxification. Searches for “carbon monoxide” and “CO detoxification” found no passage supporting that claim in our copy. (LLM, conf=0.75)
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Self-citation
- Authors
- Berney, M., Greening, C., Conrad, R., Jacobs, W. R., & Cook, G. M.
- Affiliations
- University of Otago (NZ)
- Max Planck Institute for Terrestrial Microbiology (DE)
- Albert Einstein College of Medicine (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-07-21
- Volume
- 111
- Issue
- 31
- Pages
- 11479-11484
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4128101
- OpenAlex
- W2088139692
- Cited by
- 142
- References
- 51
- Citations by year
- 2026: 14 · 2025: 8 · 2024: 23 · 2023: 14 · 2022: 13 · 2021: 12 · 2020: 12 · 2019: 18 · 2018: 3 · 2017: 7 · 2016: 10 · 2015: 4 · 2014: 4
- FWCI
- 2.75
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- University of Otago
- Royal Society
- Royal Society Te Apārangi
- Max-Planck-Institut für Terrestrische Mikrobiologie
- National Institutes of Health (AI26170)
- National Institute of Allergy and Infectious Diseases (R01AI026170, AI-26170, R01AI097548, R37AI026170)
- Otago School of Medical Sciences
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
- Keywords
- Mycobacterium smegmatis, fermentative hydrogen production, hypoxia adaptation, reductive stress, [NiFe] hydrogenase, NAD+/NADH ratio, anaerobic respiration, aerobic respiration, oxygen sensing, soil actinomycetes, metabolic switch, hydrogen recycling
- MeSH terms
- Aerobiosis, Anaerobiosis, Bacteria, Anaerobic, Bacterial Proteins, Base Sequence, Electrons, Fermentation, Homeostasis, Hydrogen, Hydrogenase, Models, Biological, Molecular Sequence Data, Oxidation-Reduction, Oxygen, Soil Microbiology, Stress, Physiological, Transcription, Genetic, Gene Expression Regulation, Bacterial, Regulon, Mycobacterium smegmatis, Intracellular Space, Microbial Viability
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