When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence

Lu, Zheng; Imlay, James A.

doi:10.1038/s41579-021-00583-y

Cited by 318Redox biology and oxidative stressBacterial Genetics and BiotechnologyMetal-Catalyzed Oxygenation Mechanisms

When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence

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Lu, Zheng, Imlay, James A.·2021·Nature Reviews Microbiology

DOI 10.1038/s41579-021-00583-yPMC PMC9191689

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Abstract

The defining trait of obligate anaerobes is that oxygen blocks their growth, yet the underlying mechanisms are unclear. A popular hypothesis was that these microorganisms failed to evolve defences to protect themselves from reactive oxygen species (ROS) such as superoxide and hydrogen peroxide, and that this failure is what prevents their expansion to oxic habitats. However, studies reveal that anaerobes actually wield most of the same defences that aerobes possess, and many of them have the capacity to tolerate substantial levels of oxygen. Therefore, to understand the structures and real-world dynamics of microbial communities, investigators have examined how anaerobes such as Bacteroides, Desulfovibrio, Pyrococcus and Clostridium spp. struggle and cope with oxygen. The hypoxic environments in which these organisms dwell - including the mammalian gut, sulfur vents and deep sediments - experience episodic oxygenation. In this Review, we explore the molecular mechanisms by which oxygen impairs anaerobes and the degree to which bacteria protect their metabolic pathways from it. The emergent view of anaerobiosis is that optimal strategies of anaerobic metabolism depend upon radical chemistry and low-potential metal centres. Such catalytic sites are intrinsically vulnerable to direct poisoning by molecular oxygen and ROS. Observations suggest that anaerobes have evolved tactics that either minimize the extent to which oxygen disrupts their metabolism or restore function shortly after the stress has dissipated.

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Both abiotic and enzymatic reactions to pyruvate synthesis along the acetyl-CoA pathway are extremely O2-sensitive due to FeS clusters in electron transfer and other radical-generating reactions.
“Second, both abiotic [90] and enzymatic reactions to pyruvate synthesis along the acetyl‐CoA pathway are extremely O2‐sensitive due to the involvement of FeS clusters in electron transfer and other radical‐generating reactions [91, 92]”
From Evidence for corrin biosynthesis in the last universal common ancestor (2025) · cites this paper as [92]
In “O₂ disrupts low-potential metal centres” (page unavailable), the paper reports that oxygen inactivates the iron–sulfur clusters of pyruvate:ferredoxin oxidoreductase. It describes this enzyme converting pyruvate to acetyl-CoA, not synthesizing pyruvate along an acetyl-CoA pathway; the separately cited abiotic reactions are not established by this source. (LLM, conf=0.87)
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Authors: Lu, Z., & Imlay, J. A.
Affiliations: Shantou University (CN)
University of Illinois Urbana-Champaign (US)
Corresponding author: Lu, Zheng
Imlay, James A.
ORCID: Lu, Zheng
Imlay, James A.
Venue: Nature Reviews Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2021-06-28
Volume: 19
Issue: 12
Pages: 774-785
ISSN: 1740-1526 (ISSN-L)
1740-1534
DOI: 10.1038/s41579-021-00583-y
PMC: PMC9191689
OpenAlex: W3174803191
Cited by: 318
References: 139
Citations by year: 2026: 68 · 2025: 86 · 2024: 67 · 2023: 51 · 2022: 41 · 2021: 5
FWCI: 4.30
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Reviews Microbiology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of General Medical Sciences (R37GM049640, R01GM049640, R01GM141252)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
Keywords: obligate anaerobes, oxygen toxicity, reactive oxygen species, antioxidant defense, superoxide, hydrogen peroxide, oxygen tolerance, Bacteroides, Desulfovibrio, Pyrococcus, Clostridium, low oxygen environment, anaerobic metabolism, microbial communities
MeSH terms: Anaerobiosis, Bacteria, Anaerobic, Bacteroides, Clostridium, Desulfovibrio, Hydrogen Peroxide, Oxygen, Superoxides, Reactive Oxygen Species, Pyrococcus

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When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence

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