Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 1

    Cody, G. D. et al. Primordial carbonylated iron–sulfur compounds and the synthesis of pyruvate. Science 289, 1337–1340 (2000).

    CAS  PubMed  Article  Google Scholar 

  2. 2

    Aylward, N. & Bofinger, N. The reactions of methanimine and cyanogen with carbon monoxide in prebiotic molecular evolution on earth. Orig. Life Evol. Biosph. 31, 481–500 (2001).

    CAS  PubMed  Article  Google Scholar 

  3. 3

    Miyakawa, S., Yamanashi, H., Kobayashi, K., Cleaves, H. J. & Miller, S. L. Prebiotic synthesis from CO atmospheres: implications for the origins of life. Proc. Natl Acad. Sci. USA 99, 14628–14631 (2002). References 1–3 provide insights into the possible roles of CO in primordial organic syntheses.

    CAS  PubMed  Article  Google Scholar 

  4. 4

    Lellouch, E. et al. Carbon monoxide in Jupiter after the impact of comet Shoemaker-Levy 9. Planet. Space Sci. 45, 1203–1212 (1997).

    CAS  Article  Google Scholar 

  5. 5

    Spyromilio, J., Leibundgut, B. & Gilmozzi, R. Carbon monoxide in type II Supernovae. Astron. Astrophys. 376, 188–193 (2001).

    CAS  Article  Google Scholar 

  6. 6

    Khalil, M. A. K. & Rasmussen, R. A. Carbon monoxide in the Earth's atmosphere: indications of a global increase. Nature 332, 242–245 (1988).

    CAS  Article  Google Scholar 

  7. 7

    Zhang, R., Wang, M. & Ren, L. Long-term trends of carbon monoxide inferred using a two-dimensional model. Chemosphere 3, 123–132 (2001).

    CAS  Google Scholar 

  8. 8

    Meyer, O. & Schlegel, H. G. Biology of aerobic carbon monoxide-oxidizing bacteria. Ann. Rev. Microbiol. 37, 277–310 (1983).

    CAS  Article  Google Scholar 

  9. 9

    Cypionka, H., van Verseveld, H. W. & Stouthamer, A. H. Proton translocation coupled to carbon monoxide-insensitive and sensitive electron transport in Pseudomonas carboxydovorans. FEMS Microbiol. Lett. 22, 209–213 (1984).

    CAS  Article  Google Scholar 

  10. 10

    Yoshida, T., Noguchi, M. & Kikuchi, G. The step of carbon monoxide liberation in the sequence of heme degradation catalyzed by the reconstituted microsomal heme oxygenase system. J. Biol. Chem. 257, 9345–9348 (1982).

    CAS  PubMed  Google Scholar 

  11. 11

    Sato, K. et al. Carbon monoxide generated by heme-oxygenase-1 suppresses the rejection of mouse-to-rat cardiac transplants. J. Immunol. 166, 185–194 (2001).

    Google Scholar 

  12. 12

    Verma, A., Hirsch, D. J., Glatt, C. E., Ronnett, G. V. & Snyder, S. H. Carbon monoxide: a putative neural messanger. Science 259, 381–384 (1993).

    CAS  PubMed  Article  Google Scholar 

  13. 13

    Zakhary, R. et al. Targeted gene deletion of heme oxygenase 2 reveals neural role for carbon monoxide. Proc. Natl Acad. Sci. USA 94, 14848–14853 (1997).

    CAS  PubMed  Article  Google Scholar 

  14. 14

    Mancuso, C., Tringali, G., Grossman, A., Preziosi, P. & Navarra, P. The generation of nitric oxide and carbon monoxide produces opposite effects on the release of immunoreactive interleukin-1 b from the rat hypothalamus in vitro: evidence for the involvement of different signaling pathways. Endocrinol. 139, 1031–1037 (1998).

    CAS  Article  Google Scholar 

  15. 15

    Xue, L. et al. Carbon monoxide and nitric oxide as co-neurotransmitters in the enteric nervous system: evidence from genomic deletion of biosynthetic enzymes. Proc. Natl Acad. Sci. USA 97, 1851–1855 (2000). References 10–15 document the importance of CO production by haem oxygenase-1 and CO-based signalling in animals, and summarize a potential application for reducing rejection of transplanted organs.

    CAS  PubMed  Article  Google Scholar 

  16. 16

    Svetlichny, V. et al. Carboxydothermus hydrogenoformans gen. nov., sp. nov., a CO-utilizing thermophilic anaerobic bacterium from hydrothermal environments of Kunashir Island. Syst. Appl. Microbiol. 14, 254–260 (1991).

    Article  Google Scholar 

  17. 17

    Klenk, H.-P. et al. The complete genome sequence of the hyperthermophilic sulphate-reducing archaeon Archaeoglobus fulgidus. Nature 390, 364–370 (1997).

    CAS  PubMed  Article  Google Scholar 

  18. 18

    Sokolova, T. G. et al. The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 8, 317–323 (2004). This reference describes an anaerobic CO oxidizer that might be representative of an early mode of metabolism at hydrothermal vents.

    CAS  PubMed  Article  Google Scholar 

  19. 19

    Wu, M. et al. Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydrogenoformans Z-2901. PLOS Genetics 1, 563–574 (2005).

    CAS  Article  Google Scholar 

  20. 20

    Lilley, M. D., de Angelis, M. A. & Gordon, L. I. CH4, H2, CO and N2O in submarine hydrothermal vent waters. Nature 300, 48–49 (1982).

    CAS  Article  Google Scholar 

  21. 21

    Crutzen, P. J. & Gidel, L. T. A two-dimensional photochemical model of the atmosphere: the tropospheric budgets of the anthropogenic chlorocarbons, CO, CH4, CH3Cl and the effect of various NOx sources on tropospheric ozone. J. Geophys. Res. 88, 6641–6661 (1983).

    CAS  Article  Google Scholar 

  22. 22

    Hendrickson, O. Q. & Kubiseski, T. Soil microbial activity at high levels of carbon monoxide. J. Environ. Qual. 20, 675–678 (1991).

    Article  Google Scholar 

  23. 23

    Bender, M. & Conrad, R. Microbial oxidation of methane, ammonium and carbon monoxide, and turnover of nitrous oxide and nitric oxide in soils. Biogeochem. 27, 97–112 (1994).

    CAS  Article  Google Scholar 

  24. 24

    Conrad, R. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, OCS, N2O and NO). Microbiol. Rev. 60, 609–640 (1996). This reference provides a thorough review of CO and other gases produced and consumed in soils.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

    Kuhlbusch, T. A. J., Zepp, R. G., Miller, W. L. & Burke, R. A. Jr. Carbon monoxide fluxes of different soil layers in upland Canadian boreal forests. Tellus 50, 353–365 (1998).

    Article  Google Scholar 

  26. 26

    Moxley, J. M. & Smith, K. A. Factors affecting utilization of CO by soils. Soil Biol. Biochem. 30, 65–79 (1997).

    Article  Google Scholar 

  27. 27

    Sanhueza, E., Dong, Y., Scharffe, D., Lobert, J. M. & Crutzen, P. J. Carbon monoxide. Tellus 50, 51–58 (1998).

    Article  Google Scholar 

  28. 28

    King, G. M. Attributes of atmospheric carbon monoxide oxidation by Maine forest soils. Appl. Environ. Microbiol. 65, 5257–5264 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29

    Whalen, S. C. & Reeburgh, W. S. Carbon monoxide consumption in upland boreal forest soils. Soil Biol. Biochem. 33, 1329–1338 (2001).

    CAS  Article  Google Scholar 

  30. 30

    Khalil, M. A. K. Atmospheric carbon monoxide. Chemosphere 1, 9–11 (1999). This paper presents a consensus budget for atmospheric CO sources and sinks.

    Google Scholar 

  31. 31

    Hino, S. & Tauchi, H. Production of carbon monoxide from aromatic amino acids by Morganella morganii. Arch. Microbiol. 148, 167–171 (1987).

    CAS  Article  Google Scholar 

  32. 32

    Conrad, R., Schütz, H. & Seiler, W. Emission of carbon monoxide from submerged rice fields into the atmosphere. Atmos. Environ. 22, 821–823 (1988).

    CAS  Article  Google Scholar 

  33. 33

    Wray, J. W. & Abeles, R. H. A bacterial enzyme that catalyzes formation of carbon monoxide. J. Biol. Chem. 268, 21466–21469 (1993).

    CAS  PubMed  Google Scholar 

  34. 34

    Tarr, M. A., Miller, W. L. & Zepp, R. G. Direct carbon monoxide production from plant matter. J. Geophys. Res. 100, 11403–11413 (1995).

    CAS  Article  Google Scholar 

  35. 35

    Schade, G. W. & Crutzen, P. J. CO emissions from degrading plant matter. (II). Estimate of a global source strength. Tellus 51, 909–918 (1999).

    Article  Google Scholar 

  36. 36

    King, G. M. Aspects of carbon monoxide production and oxidation by marine macroalgae. Mar. Ecol. Prog. Ser. 224, 69–75 (2001).

    CAS  Article  Google Scholar 

  37. 37

    King, G. M. & Crosby, H. Impacts of plant roots on soil CO cycling and soil-atmosphere exchange. Global Change Biol. 8, 1–9 (2002). This study documents the production of CO by plant roots and associated oxidation by rhizosphere bacteria.

    Article  Google Scholar 

  38. 38

    Kieber, D. J., McDaniel, J. & Mopper, K. Photochemical source of biological substrates in sea water: implications for carbon cycling. Nature 341, 637–639 (1989).

    CAS  Article  Google Scholar 

  39. 39

    Valentine, R. L. & Zepp, R. G. Formation of carbon monoxide from the photodegradation of terrestrial dissolved organic carbon in natural waters. Environ. Sci. Technol. 27, 409–412 (1993). This study describes the mechanisms and significance of photochemical CO production in aquatic systems.

    CAS  Article  Google Scholar 

  40. 40

    Bates, T. S., Kelly, K. C., Johnson, J. E. & Gammon, R. H. Regional and seasonal variations in the flux of oceanic carbon monoxide to the atmosphere. J. Geophys. Res. 100, 23093–23101 (1995).

    CAS  Article  Google Scholar 

  41. 41

    Miller, W. L. & Zepp, R. G. Photochemical production of dissolved inorganic carbon from terrestrial organic matter: significance to the oceanic organic carbon cycle. Geophys. Res. Lett. 22, 417–420 (1995).

    CAS  Article  Google Scholar 

  42. 42

    Zuo, Y. & Jones, R. D. Formation of carbon monoxide by photolysis of dissolved marine organic material and its significance in the carbon cycling of the oceans. Naturwissenschaften 82, 472–474 (1995).

    Article  Google Scholar 

  43. 43

    Haan, D., Zuo, Y., Gros, V. & Brenninkmeijer, C. A. M. Photochemical production of carbon monoxide in snow. J. Atmos. Chem. 40, 217–230 (2001).

    CAS  Article  Google Scholar 

  44. 44

    Zafiriou, O. C., Andrews, S. S. & Wang, W. Concordant estimates of oceanic carbon monoxide source and sink processes in the Pacific yield a balanced global 'blue-water' CO budget. Global Biogeochem. Cyc. 17, 1–13 (2003). This study provides the best current estimates of CO dynamics in the marine water column.

    Article  CAS  Google Scholar 

  45. 45

    Conrad, R. & Seiler, W. Role of microorganisms in the consumption and production of atmospheric carbon monoxide by soil. Appl. Environ. Microbiol. 40, 437–445 (1980).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46

    Conrad, R. & Seiler, W. Characteristics of abiological carbon monoxide formation from soil organic matter, humic acids, and phenolic compounds. Environ. Sci. Technol. 19, 1165–1169 (1985).

    CAS  PubMed  Article  Google Scholar 

  47. 47

    Moxley, J. M. & Smith, K. A. Carbon monoxide production and emission by some Scottish soil. Tellus 50, 151–162 (1998).

    Article  Google Scholar 

  48. 48

    King, G. M. Microbial CO consumption in salt marsh sediments. FEMS Microbiol. Ecol. (in the press).

  49. 49

    Lu, Y. & Khalil, M. A. K. Methane and carbon monoxide in OH chemistry: the effects of feedbacks and reservoirs generated by the reactive products. Chemosphere 26, 641–655 (1993). This paper describes interactions between CO, methane and hydroxyl radicals and their impacts on atmospheric chemistry.

    CAS  Article  Google Scholar 

  50. 50

    Bergamaschi, P., Hein, R., Heimann, M. & Crutzen, P. J. Inverse modeling of the global CO cycle. J. Geophys. Res. 105, 1909–1927 (2000).

    CAS  Article  Google Scholar 

  51. 51

    Daniel, J. S. & Solomon, S. On the climate forcing of carbon monoxide. J. Geophys. Res. 103, 13249–13260 (1998). This study identifies the indirect climate forcing or greenhouse effects of atmospheric CO.

    CAS  Article  Google Scholar 

  52. 52

    King, G. M. Characteristics and significance of atmospheric carbon monoxide consumption by soils. Chemosphere 1, 53–63 (1999).

    CAS  Google Scholar 

  53. 53

    Conrad, R., Meyer, O. & Seiler, W. Role of carboxydobacteria in consumption of atmospheric carbon monoxide by soil. Appl. Environ. Microbiol. 42, 211–215 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54

    Hardy, K. R. & King, G. M. Enrichment of high-affinity CO oxidizers in Maine forest soil. Appl. Environ. Microbiol. 67, 3671–3676 (2001). This study describes the first isolation of a CO oxidizer with uptake kinetics consistent with those of soil.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. 55

    del Moral, R. & Clampitt, C. A. Growth of native plant species on recent volcanic substrates from Mount St. Helens. Am. Midl. Nat. 114, 374–383 (1985).

    Article  Google Scholar 

  56. 56

    Lorite, M. J., Tachil, J., Sanjuan, J., Meyer, O. & Bedmar, E. J. Carbon monoxide dehydrogenase activity in Bradyrhizobium japonicum. Appl. Environ. Microbiol. 68, 1871–1876 (2000). This paper documents CO use by B. japonicum USDA 110, which possesses a form II putative CODH, but not a form I CODH.

    Article  Google Scholar 

  57. 57

    King, G. M. Molecular and culture based analyses of aerobic carbon monoxide oxidizer diversity. Appl. Environ. Microbiol. 69, 7257–7265 (2003). This study provides the first description of carboxydovores and PCR-based approaches for analysis of coxL genes.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. 58

    Davidova, M. N., Tarasova, N. B., Mukhitova, F. K. & Karpilova, I. U. Carbon monoxide in metabolism of anaerobic bacteria. Can. J. Microbiol. 40, 417–425 (1993).

    Article  Google Scholar 

  59. 59

    Roberts, G. P., Thorsteinsson, M. V., Kerby, R. L., Lanzilotta, W. N. & Poulos, T. CooA: a heme-containing regulatory protein that serves as a specific sensor of both carbon monoxide and redox state. Prog. Nucleic Acid Res. 67, 35–63 (2001).

    CAS  Article  Google Scholar 

  60. 60

    Voordouw, G. Carbon monoxide cycling by Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 184, 5903–5911 (2002).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. 61

    Ragsdale, S. W. Life with carbon monoxide. Crit. Rev. Biochem. Mol. Biol. 39, 165–195 (2004). This paper thoroughly reviews anaerobic CO metabolism.

    CAS  PubMed  Article  Google Scholar 

  62. 62

    Roberts, G. P. CO-sensing mechanisms. Microbiol. Mol. Biol. Rev. 68, 453–473 (2004).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63

    Krueger, B. & Meyer, O. Thermophilic bacilli growing with carbon monoxide. Arch. Microbiol. 139, 402–408 (1984).

    CAS  Article  Google Scholar 

  64. 64

    Lyons, C. M., Colby, J. P. & Williams, E. Isolation and characterization and autotrophic metabolism of a moderately thermophilic caboxydobacterium, Pseudomonas thermocarboxydovorans sp. nov. J. Gen. Microbiol. 130, 1097–1105 (1984).

    CAS  Google Scholar 

  65. 65

    Meyer, O. & Krueger, B. Biochemistry and physiology of aerobic carbon monoxide-utilizing bacteria. FEMS Microbiol. Lett. 39, 161–179 (1986).

    CAS  Article  Google Scholar 

  66. 66

    Auling, G. et al. Phylogenetic heterogeneity and chemotaxonomic properties of certain gram-negative aerobic carboxydobacteria. System. Appl. Microbiol. 10, 264–272 (1988).

    Article  Google Scholar 

  67. 67

    Gadkari, D., Schricker, K., Acker, G., Kroppensetdt, R. M. & Meyer, O. Streptomyces thermoautotrophicus sp. nov., a thermophilic CO- and H2-oxidizing obligate chemolithotroph. Appl. Environ. Microbiol. 56, 3727–3734 (1990). This paper describes the only known obligate CO oxidizer, a thermophilic streptomycete isolated from a smouldering coal pile.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68

    Weber, C. F. & King, G. M. Physiological, ecological and phylogenetic characterization of Stappia, a marine CO-oxidizing bacterial genus. Appl. Environ. Microbiol. (in the press).

  69. 69

    Park, S. W. et al. Growth of mycobacteria on carbon monoxide and methanol. J. Bacteriol. 185, 142–147 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. 70

    Moran, M. A. et al. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432, 910–913 (2004).

    CAS  PubMed  Article  Google Scholar 

  71. 71

    Tolli, J. D., Sievert, S. M. & Taylor, C. D. Unexpected diversity of bacteria capable of carbon monoxide oxidation in a coastal marine environment, and contribution of the Roseobacter-associated clade to total CO oxidation. Appl. Environ. Microbiol. 72, 1966–1973 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  72. 72

    Kiessling, M. & Meyer, O. Profitable oxidation of carbon monoxide or hydrogen during heterotrophic growth of Pseudomonas carboxydoflava. FEMS Microbiol. Lett. 13, 333–338 (1982).

    CAS  Article  Google Scholar 

  73. 73

    Kim, Y. J. & Kim, Y. M. Induction of carbon monoxide dehydrogenase during heterotrophic growth of Acinetobacter sp. strain JC1 DSM 3803 in the presence of carbon monoxide. FEMS Microbiol. Lett. 59, 207–210 (1989).

    CAS  Article  Google Scholar 

  74. 74

    Oremland, R. S. et al. Anaerobic oxidation of arsenite in Mono Lake water and by a facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Appl. Environ. Microbiol. 68, 4795–4802 (2002).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  75. 75

    Hoeft, S. E. et al. Alkalilimnicola ehrlechei sp. nov., a novel, arsenite-oxidizing haloalkaliphilic- proteobacterium capable of chemoautotrophic or heterotrophic growth with nitrate or oxygen as the electron acceptor. Int. J. Syst. Evol. Microbiol. (in the press).

  76. 76

    Meyer, O. & Rajagopalan, K. V. Molybdopterin in carbon monoxide oxidase from carboxydotrophic bacteria. J. Bacteriol. 157, 643–648 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 77

    Kraut, M. & Meyer, O. Plasmids in carboxydotrophic bacteria: physical and restriction analysis. Arch. Microbiol. 149, 540–546 (1988).

    CAS  Article  Google Scholar 

  78. 78

    Mörsdorf, G., Frunzke, K., Gadkari, D. & Meyer, O. Microbial growth on carbon monoxide. Biodegradation 3, 61–82 (1992). This paper provides a review of aerobic CO oxidation, including aspects of physiology and biochemistry.

    Article  Google Scholar 

  79. 79

    Schübel, U., Kraut, M., Mörsdorf, G. & Meyer, O. Molecular characterization of the gene cluster coxMSL encoding the molybdenum-containing carbon monoxide dehydrogenase of Oligotropha carboxidovorans. J. Bacteriol. 177, 2197–2203 (1995).

    PubMed  PubMed Central  Article  Google Scholar 

  80. 80

    Hänzelmann, P. & Meyer, O. Effect of molybdate and tungstate on the biosynthesis of CO dehydrogenase and the molybdopterin cytosine-dinucleotide-type of molybdenum cofactor in Hydrogenaphaga pseudoflava. Eur. J. Biochem. 255, 755–765 (1998).

    PubMed  Article  Google Scholar 

  81. 81

    Hänzelmann, P., Hofmann, B., Meisen, S. & Meyer, O. The redox centers in the molybdo iron–sulfur flavoprotein CO dehydrogenase form the thermophilic carboxidotrophic bacterium Pseudomonas thermocarboxydovorans. FEMS Microbiol. Lett. 176, 139–145 (1999).

    Article  Google Scholar 

  82. 82

    Dobbek, H., Gremer, L., Meyer, O. & Huber, R. Crystal structure and mechanism of CO dehydrogenase, a molybdo iron-sulfur flavoprotein containing S-selenylcysteine. Proc. Natl Acad. Sci. USA 96, 8884–8889 (1999).

    CAS  PubMed  Article  Google Scholar 

  83. 83

    Santiago, B., Schuebel, U., Egelseer, C. & Meyer, O. Sequence analysis, characterization and CO-specific transcription of the cox gene cluster on the megaplasmid pHCG3 of Oligotropha carboxidovorans. Gene 236, 115–124 (1999). This important paper summarizes the cox operon structure of O.carboxidovorans and other CO oxidizers, including the identification of structural and accessory genes and their roles.

    CAS  PubMed  Article  Google Scholar 

  84. 84

    Fuhrmann, S. et al. Complete nucleotide sequence of the circular megaplasmid pHCG3 of Oligotropha carboxidovorans: function in the chemolithoautotrophic utilization of CO, H2 and CO2 . Gene 322, 67–75 (2003).

    CAS  PubMed  Article  Google Scholar 

  85. 85

    Gnida, M., Ferner, R. Gremer, L., Meyer O. & Meyer-Klauke, W. A novel binuclear [CuSMo] cluster at the active site of carbon monoxide dehydrogenase: characterization by X-ray absorption spectroscopy. Biochem. 42, 222–230 (2003). This study identifies the nature of the CODH active site and, with reference 81, provides a comprehensive analysis of the structure of aerobic CODH.

    CAS  Article  Google Scholar 

  86. 86

    Bell, J. M., Colby, J. & Williams, E. CO oxidoreductase from Streptomyces strain G26 is a molybdenum hydroxylase. Biochem. J. 250, 605–612 (1988).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  87. 87

    Hille, R. Molybdenum-containing hydroxylases. Arch. Biochem. Biophys. 433, 107–116 (2005).

    CAS  PubMed  Article  Google Scholar 

  88. 88

    Pearson, D. M., O'Reilly, C., Colby, J. & Black, G. W. DNA sequence of the cut A, B and C genes, encoding the molybdenum containing hydroxylase carbon monoxide dehydrogenase from Pseudomonas thermocarboxydovorans strain C2. Biochim. Biophys. Acta 1188, 432–438 (1994).

    Article  Google Scholar 

  89. 89

    Kang, B. S. & Kim, Y. M. Cloning and molecular characterization of the genes for carbon monoxide dehydrogenase and localization of molybdopterin, flavin adenine dinucleotide, and iron–sulfur centers in the enzyme of Hydrogenophaga pseudoflava. J. Bacteriol. 181, 5581–5590 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. 90

    Kaneko, T. et al. Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res. 9, 189–197 (2002).

    PubMed  PubMed Central  Article  Google Scholar 

  91. 91

    Aono, S., Nakajima, H., Saito, K. & Okada, M. A novel heme protein that acts as a carbon monoxide-dependent transcriptional activator in Rhodospirillum rubrum. Biochem. Biophys. Res. Comm. 228, 752–756 (1996).

    CAS  PubMed  Article  Google Scholar 

  92. 92

    Heo, J., Halbleib, C. M. & Ludden, P. W. Redox-dependent activation of CO dehydrogenase from Rhodospirillum rubrum. Proc. Natl Acad. Sci. USA 98, 7690–7693 (2001).

    CAS  PubMed  Article  Google Scholar 

  93. 93

    Coyle, C. M. et al. Activation mechanism of the CO sensor CooA. J. Biol. Chem. 278, 35384–35393 (2003).

    CAS  PubMed  Article  Google Scholar 

  94. 94

    King, G. M. Uptake of carbon monoxide and hydrogen at environmentally relevant concentrations by mycobacteria. Appl. Environ. Microbiol. 69, 7266–7272 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. 95

    Tyson, G. W. et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428, 1–7 (2004).

    Article  CAS  Google Scholar 

  96. 96

    Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).

    CAS  Article  PubMed  Google Scholar 

  97. 97

    Scharffe, D., Hao, W. M., Donoso, L., Crutzen, P. J. & Sanhueza, E. Soil fluxes and atmospheric concentrations of CO and CH4 in the northern part of the Guyana Shield, Venezuela. J. Geophys. Res. 95, 22475–22480 (1990).

    CAS  Article  Google Scholar 

  98. 98

    Schmidt, U. & Conrad, R. Hydrogen, carbon monoxide and methane dynamics in Lake Constance. Limnol. Oceanogr. 38, 1214–1226 (1993).

    CAS  Article  Google Scholar 

  99. 99

    Rich, J. J. & King, G. M. Carbon monoxide oxidation by bacteria associated with the roots of freshwater macrophytes. Appl. Environ. Microbiol. 64, 4939–4943 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. 100

    King, G. M. & Hungria, M. Soil-atmosphere CO exchanges and microbial biogeochemistry of CO transformations in a Brazilian agriculture ecosystem. Appl. Environ. Microbiol. 68, 4480–4485 (2002).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  101. 101

    Tolli, J. D. & Taylor, C. D. Biological CO oxidation in the Sargasso Sea and in Vineyard Sound, Massachusetts. Limnol. Oceanogr. 50, 1205–1212 (2005).

    CAS  Article  Google Scholar 

  102. 102

    Holloway, T., Levy II, H. & Kasibhatla, P. Global distribution of carbon monoxide. J. Geophys. Res. 105, 12123–12147 (2000).

    CAS  Article  Google Scholar 

  103. 103

    Dunfield, K. E. & King, G. M. Molecular analysis of carbon monoxide-oxidizing bacteria associated with recent Hawaiian volcanic deposits. Appl. Environ. Microbiol. 70, 4242–4248 (2004). This study describes the first culture-independent or molecular analyses of CO oxidizers in terrestrial systems.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. 104

    Denton, M. D., Reeve, W. G., Howieson, J. G. & Coventry, D. R. Competitive abilities of common field isolates and a commercial strain of Rhizobium leguminosarum bv. trifolii for clover nodule occupancy. Soil Biol. Biochem. 35, 1039–1048 (2003).

    CAS  Article  Google Scholar 

  105. 105

    Dong, Y., Iniguez, A. L., Ahmer, B. M. M. & Triplett, E. W. Kinetics and strain specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl. Environ. Microbiol. 69, 1783–1790 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. 106

    Gage, D. J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Molec. Biol. Rev. 68, 280–300 (2004).

    CAS  Article  Google Scholar 

  107. 107

    Miethling, R., Wieland, H., Backhaus, H. & Tebbe, C. C. Variation of microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microb. Ecol. 40, 43–56 (2000).

    CAS  PubMed  Article  Google Scholar 

  108. 108

    Moulin, L., Munive, A., Dreyfus, B. & Bolvin-Masson, C. Nodulation of legumes by members of the γ-subclass of Proteobacteria. Nature 411, 948–950 (2001).

    CAS  PubMed  Article  Google Scholar 

  109. 109

    Phillips, D. A. & Streit, W. in Plant Microbe Interactions (eds Stacey, G. & Keen, N. T.) 236–271 (Chapman Hall, 1995).

    Google Scholar 

  110. 110

    Schweiger, F. & Tebbe, C. C. Effect of field inoculation with Sinorhizobium meliloti L33 on the composition of bacterial communities in rhizospheres of a target plant (Medicago sativa) and a non-target plant (Chenopodium album) — linking of 16S rRNA gene-based single-strand conformation polymorphism community profiles to the diversity of cultivated bacteria. Appl. Environ. Microbiol. 66, 3556–3565 (2000).

    Article  Google Scholar 

  111. 111

    Thorne, S. H. & Williams, H. D. Adaptation to nutrient starvation in Rhizobium leguminosarum bv. phaseoli: analysis of survival, stress resistance and changes in macromolecular synthesis during entry to and exit from stationary phase. J. Bacteriol. 179, 6894–6901 (1997).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  112. 112

    Zahran, H. H. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. Molec. Biol. Rev. 63, 968–989 (1999).

    CAS  Google Scholar 

  113. 113

    Dowling, D. N. & Broughton, W. J. Competition for nodulation of legumes. Ann. Rev. Microbiol. 40, 131–151 (1986).

    CAS  Article  Google Scholar 

  114. 114

    Bromfield, E. S. P. & Barran, L. R. Is frequency of occurrence of indigenous Rhizobium melilot i in nodules of field grown plants related to intrinsic competitiveness. Soil Biol. Biochem. 21, 608–609 (1989).

    Article  Google Scholar 

  115. 115

    Laguerre, G., Louvrier, P., Allard, M.-R. & Amarger, N. Compatibility of rhizobial genotypes within natural populations of Rhizobium leguminosarum biovar viciae for nodulation of host legumes. Appl. Environ. Microbiol. 69, 2276–2283 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. 116

    George, S. J., Ashby, G. A., Wharton, C. W. & Thorneley, R. N. F. Time-resolved binding of carbon monoxide to nitrogenase monitored by stopped-flow infared spectroscopy. J. Am. Chem. Soc. 119, 6450–6451 (1997).

    CAS  Article  Google Scholar 

  117. 117

    Wittenberg, J. B., Appleby, C. A. & Wittenberg, B. A. The kinetics of the reaction of Parasponia andersonii leghemoglobin with oxygen and carbon monoxide. J. Biol. Chem. 247, 527–531 (1971).

    Google Scholar 

  118. 118

    Martin, K. D. et al. Kinetics and thermodynamics of oxygen, CO and azide binding by the subcomponents of soybean leghemoglobin. J. Biol. Chem. 265, 19588–19593 (1990).

    CAS  PubMed  Google Scholar 

  119. 119

    Albrecht, S. L. et al. Hydrogenase in Rhizobium japonicum increases nitrogen fixation by nodulated soybeans. Science 203, 1255–1257 (1979).

    CAS  PubMed  Article  Google Scholar 

  120. 120

    Conrad, R. & Seiler, W. Field measurements of hydrogen evolution by nitrogen-fixing legumes. Soil Biol. Biochem. 11, 689–690 (1979).

    CAS  Article  Google Scholar 

  121. 121

    La Favre, J. S. & Focht, D. D. Conservation in soil of H2 liberated from N2 fixation by Hup- nodules. Appl. Environ. Microbiol. 46, 304–311 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. 122

    Popelier, F., Liessens, J. & Verstraete, W. Soil H2- uptake in relation to soil properities and rhizobial H2 production. Plant Soil 85, 85–96 (1985).

    CAS  Article  Google Scholar 

  123. 123

    Cunningham, S. D., Kapulink, Y. & Phillips, D. A. Distribution of hydrogen-metabolizing bacteria in alfalfa field soil. Appl. Environ. Microbiol. 52, 1091–1095 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. 124

    Evans, H. J., Russell, S. A., Hanus, F. J. & Ruiz-Argüeso, T. in World Crops: Cool Season Food Legumes (ed. Summerfield, R. J.) 777–792 (Kluwer Academic Publishers, Boston USA, 1988).

    Book  Google Scholar 

  125. 125

    Murillo, J., Villa, A., Chamber, M. & Ruiz-Argüeso, T. Occurrence of H2-uptake hydrogenases in Bradyrhizobium sp. (Lupinus) and their expression in nodules of Lupinus spp. and Ornithopus compressus. Plant Physiol. 89, 78–85 (1989).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. 126

    Rasche, M. E. & Arp, D. J. Hydrogen inhibition of nitrogen reduction by nitrogenase in isolated soybean nodule bacteroids. Plant Physiol. 91, 663–668 (1989).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. 127

    Navarro, R. B., Vargas, A. A. T., Schroder, E. C. & van Berkum, P. Uptake hydrogenase (Hup) in common bean (Phaseolus vulgaris) symbioses. Appl. Environ. Microbiol. 59, 4161–4165 (1993). References 119–127 show parallels between hydrogen and CO dynamics and significance in rhizobia–legume symbioses.

    CAS  PubMed  PubMed Central  Google Scholar 

  128. 128

    Jones, R. D. & Morita, R. Y. Effects of various parameters on carbon monoxide oxidation by ammonium oxidizers. Can. J. Microbiol. 30, 894–899 (1983).

    Article  Google Scholar 

  129. 129

    Jones, R. D., Morita, R. Y. & Griffiths, R. P. Method for estimating in situ chemolithotrophic ammonium oxidation using carbon monoxide oxidation. Mar. Ecol. Prog. Ser. 17, 259–269 (1984).

    CAS  Article  Google Scholar 

  130. 130

    King, G. M. Uptake of carbon monoxide and hydrogen at environmentally relevant concentrations by mycobacteria. Appl. Environ. Microbiol. 69, 7266–7272 (2003). This study indicates that atmospheric CO and hydrogen can contribute to the dynamics of microbial succession on carbon poor volcanic materials.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  131. 131

    Rodwell, T. C., Whyte, I. J. & Boyce, W. M. Evaluation of population effects of bovine tuberculosis in free-ranging African buffalo (Syncerus caffer). J. Mammal. 82, 231–238 (2001).

    Article  Google Scholar 

  132. 132

    Ayele, W. Y., Neill, S. D., Zinsstag, J., Weiss, M. G. & Pavlik, I. Bovine tuberculosis: an old disease but new threat to Africa. Int. J. Tuberc. Lung. Dis. 8, 924–937 (2004).

    CAS  PubMed  Google Scholar 

  133. 133

    Brewer, T. F. & Heymann, S. J. To control and beyond: moving towards eliminating the global tuberculosis threat. J. Epidemiol. Community Health 58, 822–825 (2006).

    Article  Google Scholar 

  134. 134

    King, G. M. Land use impacts on atmospheric carbon monoxide consumption by soils. Global Biogeochem. Cyc. 14, 1161–1172 (2000). This study summarizes relationships between land use and soil–atmosphere CO fluxes.

    CAS  Article  Google Scholar 

  135. 135

    Thompson, J. D., Gibson, T. J., Pleuniak, F., Jeanmougin, F. & Higgins, D. G. The Clustal X-Windows interface: flexible strategies for multiple sequence alignment aided by quality tools. Nucleic Acids Res. 25, 4876–4882 (1997).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  136. 136

    Swofford, D. L. PAUP: phylogenetic analysis using parsimony, Ver. 4. (Sinauer Associates, Sunderland USA, 2003).

Download references

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Gary M. King.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

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.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing