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Distribution, diversity and ecology of aerobic CO-oxidizing bacteria

Key Points

  • Carbon monoxide (CO) supports the growth and metabolism of a phylogenetically diverse group of aerobic proteobacteria. The terms carboxydotroph and carboxydovore refer to bacteria that grow or are unable to grow in environments with elevated CO concentrations (>1%), respectively.

  • Aerobic CO oxidizers use a molybdenum hydroxylase, CO dehydrogenase (CODH), to oxidize CO. CODH differs distinctly from an enzyme used by anaerobes to oxidize CO.

  • Form I (also known as OMP) CODH actively oxidizes CO and has been extensively characterized. A putative CODH, referred to as form II (also known as BMS), shares many characteristics with form I CODH, but seems to oxidize CO slowly, and might do so incidentally.

  • Genes for the form I CODH large subunit (coxL) can be readily distinguished from form II putative coxL genes by the presence of an AYXCSFR active-site motif in form I, and an AYXGAGR motif in form II. Although genomic databases for bacteria and metagenomic databases for environmental samples have helped to identify many new CO oxidizers, many genes identified as aerobic CODH genes have also been misannotated.

  • Aerobic CO oxidizers occur commonly in soils and aquatic habitats; many of these bacteria probably function as mixotrophs, using both CO and various organic substrates simultaneously. Results from organic-poor environments, such as recent volcanic deposits, indicate that CO oxidizers are important pioneering colonists and that atmospheric CO provides a significant source of energy.

  • Aerobic CO oxidizers include important human and animal pathogens, for example, Mycobacterium bovis and Mycobacterium tuberculosis, as well as important plant symbionts, for example, Bradyrhizobium japonicum and numerous other rhizobia. Both pathogens and plant symbionts might use host-derived CO as an energy source for enhanced survival.

Abstract

Numerous studies indicate that carbon monoxide (CO) participates in a broader range of processes than any other single molecule, ranging from subcellular to planetary scales. Despite its toxicity to many organisms, a diverse group of bacteria that span multiple phylogenetic lineages metabolize CO. These bacteria are globally distributed and include pathogens, plant symbionts and biogeochemically important lineages in soils and the oceans. New molecular and isolation techniques, as well as genome sequencing, have greatly expanded our knowledge of the diversity of CO oxidizers. Here, we present a newly emerging picture of the distribution, diversity and ecology of aerobic CO-oxidizing bacteria.

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Figure 1: Main natural biospheric sources and sinks for carbon monoxide.
Figure 2: Phylogenetic analysis of 16S rRNA genes, form I coxL and form II putative coxL genes from CO-oxidizing bacteria and related isolates.
Figure 3: Organization of form I cox and form II putative cox genes from selected CO-oxidizing bacteria.
Figure 4: Phlyogenetic analysis of partially translated form I coxL and form II putative coxL sequences derived from the Sargasso Sea metagenome.
Figure 5: Phlyogenetic analysis of partially translated form I coxL sequences derived from clone libraries of Hawaiian volcanic deposits.
Figure 6: CO-based interactions between nitrogen-fixing symbionts and their hosts.

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Acknowledgements

The authors were supported in part by the National Science Foundation. We thank O. Meyer, University of Bayreuth, for helpful discussions about form I and form II CODHs.

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Correspondence to Gary M. King.

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DATABASES

Entrez Genome Project

Acidobacterium bacterium Ellin345

Alkalilimnicola ehrlichei MLHE-1

Arthrobacter sp. FB24

Bradyrhizobium japonicum USDA 110

Burkholderia xenovorans LB400

Carboxydothermus hydrogenoformans

Mesorhizobium loti 303099

Mycobacterium bovis

Mycobacterium tuberculosis

Nocardioides sp. JS614

Silicibacter pomeroyi

Sinorhizobium meliloti 1021

Solibacter usitatus

Stappia aggregata

FURTHER INFORMATION

Ribosomal Database Project

Glossary

Cosmochemical reaction

A chemical reaction that takes place external to the surfaces of stars and planets.

Troposphere

The lower region of Earth's atmosphere, extending to an altitude of about 15 km.

Organic substrate

A molecule that consists of carbon in a reduced state, which is used as a source of energy and cell mass by heterotrophs.

Mixotrophic metabolism

The simultaneous use of reduced inorganic and organic substrates for cellular activity.

Gas chromatographic analysis

A procedure for determining the components of mixtures of volatile substances based on separation in a column and detection by one or more methods.

Moderate thermophile

An organism with growth optima between 45–80 °C.

Phyllosphere

The external surfaces of above-ground plant tissues that support epiphytic microbial growth.

Moderate alkaliphile

An organism with growth optima in alkaline media with a pH between 8–10.

Extreme halophile

An organism with growth optima in salt solutions with a concentration >1 M.

Psychrophile

An organism with growth optima <10 °C.

Hyperthermophile

An organism with growth optima >80–85 °C.

Rhizosphere

The soil zone immediately surrounding a plant root system.

Aquatic macrophyte

A rooted, vascular plant that grows preferentially in permanently or ephemerally flooded sediments or soils.

Rhizobia

A group of α-proteobacteria composed of nitrogen-fixing plant symbionts in the genera Azorhizobium, Bradyrhizobium, Mesorhizobium, Rhizobium and Sinorhizobium.

Bacteroid

The rod-like, nitrogen-fixing symbionts (rhizobia) that occur within legume root nodules.

STAR-FISH

Substrate-tracking autoradiography-fluorescent in situ hybridization. A method for visualizing which members of a specific microbial assemblage use a specific substrate.

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King, G., Weber, C. Distribution, diversity and ecology of aerobic CO-oxidizing bacteria. Nat Rev Microbiol 5, 107–118 (2007). https://doi.org/10.1038/nrmicro1595

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