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Shallow breathing: bacterial life at low O2

Nature Reviews Microbiology volume 11, pages 205–212 (2013)Cite this article

Subjects

Key Points

  • Microoxic environments are prevalent in nature, including in aquatic, terrestrial and host-associated environments.

  • Although a subset of bacteria known as microaerophiles grow optimally under microoxic conditions, many bacteria that have traditionally been characterized as aerobes or anaerobes also occupy these environments. All microorganisms that are capable of respiring low levels of O2 are defined as microaerobes.

  • Cytochrome oxidases with a high affinity for O2 are common in phylogenetically diverse bacterial genomes (∼70% of species surveyed) and provide microaerobes with access to scarce supplies of O2.

  • Analysis of shotgun metagenomes reveals a widespread occurrence of genes encoding high-affinity oxidases, providing intriguing evidence that supports the importance of microaerobic metabolism.

  • Understanding the physiology and ecology of microaerobes in low-O2 environments is integral to advancing our understanding of host-associated microbiomes, for both colonization and pathogen invasion.

  • Advances in both O2-sensing technologies and microoxic cultivation will provide opportunities for the exploration of the local and global impacts of microaerobes.

Abstract

Competition for molecular oxygen (O2) among respiratory microorganisms is intense because O2 is a potent electron acceptor. This competition leads to the formation of microoxic environments wherever microorganisms congregate in aquatic, terrestrial and host-associated communities. Bacteria can harvest O2 present at low, even nanomolar, concentrations using high-affinity terminal oxidases. Here, we report the results of surveys searching for high-affinity terminal oxidase genes in sequenced bacterial genomes and shotgun metagenomes. The results indicate that bacteria with the potential to respire under microoxic conditions are phylogenetically diverse and intriguingly widespread in nature. We explore the implications of these findings by highlighting the importance of microaerobic metabolism in host-associated bacteria related to health and disease.

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Figure 1: The distribution of terminal oxidases in bacterial genomes linked to physiological groups of microorganisms and their distribution in an O2 gradient.
Figure 2: Distribution of terminal oxidase genes in shotgun metagenomes.
Figure 3: Distribution of high-affinity terminal oxidase genes across terrestrial landscapes following release of the land from agriculture.

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Acknowledgements

The authors thank J. Breznak for seminal conversations about the ecological importance of microaerobes; K. D. Noel and C. Waldron for critical reading of this manuscript; T. Teal and B. Klahn for their expert assistance with the genomic and metagenomic analyses; and members of the Schmidt laboratory for many helpful discussions concerning the potential consequences of microaerobes and microoxic environments. This work was supported by grants from the US National Institutes of Health (R01 HG004906 and UH3 DK083993) and the US National Science Foundation (MCB 0731913 and DEB 1027253).

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  1. Rachel L. Morris

    Present address: Present address: Department of Internal Medicine, University of Michigan, Ann Arbor, Michigan 48109, USA.,

  2. Thomas M. Schmidt

    Present address: Present address: Department of Internal Medicine, Department of Microbiology and Immunology, and Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA.,

Authors and Affiliations

  1. Department of Microbiology and Molecular Genetics, 6180 Biomedical Physical Sciences, Michigan State University, East Lansing, 48824, Michigan, USA

    Rachel L. Morris & Thomas M. Schmidt

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Supplementary information

Supplementary informtation S1 (table)

Occurrence of high-affinity oxidase genes in bacterial genomes. (PDF 201 kb)

Supplementary informtation S2 (box)

Metagenome Analysis of Terminal Oxidase Genes (PDF 219 kb)

Supplementary informtation S3 (table)

MG-RAST accession numbers for the metagenomes in Figures 2 and 3. (PDF 201 kb)

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Morris, R., Schmidt, T. Shallow breathing: bacterial life at low O2. Nat Rev Microbiol 11, 205–212 (2013). https://doi.org/10.1038/nrmicro2970

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