Chapter 10 : Microaerobic Physiology: Aerobic Respiration, Anaerobic Respiration, and Carbon Dioxide Metabolism

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In aerobic respiration, electron transfer is to oxygen (more correctly, the dioxygen molecule), which is reduced to water with concomitant, coupled ion translocation and generation of an electrochemical gradient. In anaerobic respiration, electron transfer is to a molecule other than oxygen or to an ionic species, again coupled to generation of an electrochemical gradient. This chapter is concerned primarily with substrate oxidations and the use of oxygen as electron acceptor. It examines the evidence for facultative respiration in and considers the extent to which the respiratory pathways of this bacterium can be gleaned from the somewhat limited biochemical evidence presently available, and from comparisons with mitochondrial and bacterial paradigms. Oxidative stress responses are coordinated by a number of global regulatory proteins. In , alkylhydroperoxide reductase, catalase, and superoxide dismutase have been particularly implicated in the enzymatic destruction of toxic oxidants and are discussed in the chapter. is generally regarded as a microaerophile, but the bacterium also requires an elevated level of atmospheric CO for optimal growth.

Citation: Kelly D, Poole R, Hughes N. 2001. Microaerobic Physiology: Aerobic Respiration, Anaerobic Respiration, and Carbon Dioxide Metabolism, p 113-124. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch10
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Figure 1

Hypothetical arrangement of the major components of the respiratory chains of Reduced substrates (DH) are oxidized (to D) via membrane-bound or membrane-associated dehydrogenases. Integral membrane oxidoreductases include an NDH-1 complex (Nuo), the electron donor to which is unknown, and hydrogenase (Hya, also termed Hyd). Peripherally associated oxidoreductases include (among several others) malate:quinone oxidoreductase (Mqo). Reducing equivalents from all these substrates reduce the sole quinone, menaquinone-6, in the lipid bilayer of the inner membrane. Menaquinol reduces the trimeric cytochrome complex (Pet), which in turn reduces periplasmic cytochrome (). Cytochrome is reoxidized by the sole terminal oxidase of the Cco (or Fix) type, cytochrome (or ) Cytochrome may also be reoxidized by hydrogen peroxide in the periplasm through the activity of cytochrome peroxidase (CCP). Fumarate reductase (Frd) catalyzes electron transfer from menaquinol to fumarate as terminal acceptor. The reactions catalyzed by CcO, CCP, FrdA, Mqo, and Nuo show substrate/product conversions. The other arrows indicate directions of electron transfer.

Citation: Kelly D, Poole R, Hughes N. 2001. Microaerobic Physiology: Aerobic Respiration, Anaerobic Respiration, and Carbon Dioxide Metabolism, p 113-124. In Mobley H, Mendz G, Hazell S (ed), . ASM Press, Washington, DC. doi: 10.1128/9781555818005.ch10
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1. Alderson, J.,, C. L. Clayton,, and D. J. Kelly. 1997. Investigations into the aerobic respiratory chain of Helicobacter pylori. Gut 41( S1): A7.
2. Alderson, J.,, and D. J. Kelly. Unpublished data.
3. Aim, R. A.,, L.-S. Lee,, D. T. Moir,, B. L. King,, E. D. Brown,, P. C. Doig,, D. R. Smith,, B. Noonan,, B. C. Guild,, B. L. de Jonge,, G. Carmel,, P. J. Tummino,, A. Caruso,, M. Uria-Nickelson,, D. M. Mills,, C. Ives,, R. Gibson,, D. Merberg,, S. D. Mills,, Q. Jiang,, D. E. Taylor,, G. F. Vovis,, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176 180.
4. Baer, W.,, H. Koopman,, and S. Wagner. 1993. Effects of substances inhibiting or uncoupling respiratory chain phosphorylation of Helicobacter pylori. Zentralbl. Bakteriol. 280: 253 258.
5. Baillon, M. L.,, A. H. van Vliet,, J. M. Ketley,, C. Constaninidou,, and C. W. Penn. 1999. An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J. Bacteriol. 181: 4798 4804.
6. Beckman, D. L.,, D. R. Trawick,, and R. G. Kranz. 1992. Bacterial cytochromes c biogenesis. Genes Dev. 6: 268 283.
7. Bereswill, S.,, O. Neuner,, S. Strobel,, and M. Kist. 2000. Identification and molecular analysis of superoxide dismutase isoforms in Helicobacter pylori. FEMS Microbiol. Lett. 183: 241 245.
8. Burns, B. P.,, S. L. Hazell,, and G. L. Mendz. 1995. Acetyl-CoA carboxylase activity in Helicobacter pylori and the requirement of increased C0 2 for growth. Microbiology 141: 3113 3118.
9. Carlone, G. M.,, and F. A. L. Anet. 1983. Detection of menaqui-none-6 and a novel methyl-substituted menaquinone-6 in Campylobacter jejuni and Campylobacter fetus subsp. fetus. J. Gen. Microbiol. 129: 3385 3393.
10. Chalk, P. A.,, A. D. Roberts,, and W. M. Blows. 1994. Metabolism of pyruvate and glucose by intact cells of H. pylori studied by I3C-NMR spectroscopy. Microbiology 140: 2085 2902.
11. Chalk, P. A.,, A. D. Roberts,, A. A. Davison,, D. J. Kelly,, and P. J. White,. 1997. The use of NMR to study the metabolism of Helicobacter pylori, p. 69 80. In C. L. Clayton, and H. L. T. Mobley (ed.), Methods in Molecular Medicine—Helicobacter pylori Protocols. Humana Press Inc., New York, N.Y..
12. Chang, H. T.,, S. W. Marcelli,, A. A. Davison,, P. A. Chalk,, R. K. Poole,, and R. J. Miles. 1995. Kinetics of substrate oxidation by whole cells and cell membranes of Helicobacter pylori. FEMS Microbiol. Lett. 129: 33 38.
13. Chen, M.,, L. P. Andersen,, L. Zhai,, and A. Kharazmi. 1999. Characterization of the respiratory chain of Helicobacter pylori. FEMS Immunol. Med. Microbiol. 24: 169 174.
14. Collins, M. D.,, M. Costas,, and R. J. Owens. 1984. Isoprenoid quinone composition of representatives of the genus Campylobacter. Arch. Microbiol. 137: 168 170.
15. D'mello, R.,, S. Hill,, and R. K. Poole. 1996. The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition. Microbiology 142: 755 763.
16.. Deshpande, M.,, E. Calenoff,, and L. Daniels. 1995. Rapid large-scale growth of Helicobacter pylori in flasks and fermentors. Appl. Environ. Microbiol. 61: 2431 2435.
17. Doig, P.,, B. L. de Jonge,, R. A. Aim,, E. D. Brown,, M. Uria-Nickelsen,, B. Noonan,, S. D. Mills,, P. Tummino,, G. Carmel,, B. C. Guild,, D. T. Moir,, G. F. Vovis,, and T. J. Trust. 1999. Helicobacter pylori physiology predicted from genomic comparison of two strains. Microbiol. Mol. Biol. Rev. 63: 675 707.
18. Evans, D. J., Jr.,, and D. G. Evans. 1997. Identification of a formate dehydrogenase associated cytochrome C553 in Helicobacter pylori. Gut 41( Suppl.): A6.
19. Finel, M. 1998. Does NADH play a central role in energy metabolism in Helicobacter pylori? Trends Biochem. Sci. 23: 412 414.
20. Fischer, H.-M. 1994. Genetic regulation of nitrogen fixation in Rhizobia. Microbiol. Rev. 58: 352 386.
21. Ge, Z.,, Q. Jiang,, M. S. Kalisiak,, and D. E. Taylor. 1997. Cloning and functional characterization of Helicobacter pylori fumarate reductase operon comprising three structural genes coding for subunits C, A and B. Gene 204: 227 234.
22. Gilbert, J. V.,, J. Ramakrishna,, F. W. Sunderman, Jr.,, A. Wright,, and A. G. Plaut. 1995. Protein Hpn: cloning and characterisation of a histidine-rich metal binding polypeptide in Helicobacter pylori and Helicobacter mustelae. Infect, lmmun. 62: 2682 2688.
23. Goldman, B. S.,, and R. G. Kranz. 1998. Evolution and horizontal transfer of an entire biosynthetic pathway for cytochrome c biogenesis: Helicobacter, Deinococcus, Archae, and more. Mol. Microbiol. 27: 871 874.
24. Goodhew, C. F.,, I. B. H. Wilson,, D. J. B. Hunter,, and G. W. Pettigrew. 1990. The cellular location and specificity of bacterial cytochrome c peroxidases. Biochem. J. 271: 707 712.
25. Goodhew, C. F.,, A. B. EIKurdi,, and G. Pettigrew. 1988. The microaerophilic respiration of Campylobacter mucosalis. Bio-chim. Biophys. Acta 933: 114 123.
26. Hazell, S. L.,, D. J. Evans,, and D. Y. Graham. 1991. Helicobacter pylori catalase. J. Gen. Microbiol. 137: 57 61.
27. Hoffman, P. S.,, A. Goodwin,, J. Johnsen,, K. Magee,, and S. Veldhuyzen van Zanten. 1996. Metabolic activities of metroni-dazole-sensitive and resistant strains of Helicobacter pylori: repression of pyruvate oxidoreductase and expression of isocitrate lyase activity correlate with resistance. J. Bacteriol. 178: 4822 4829.
28. Hughes, N. J.,, P. A. Chalk,, C. L. Clayton,, and D. J. Kelly. 1995. Identification of carboxylation enzymes and characterization of a novel four-subunit pyruvate: flavodoxin oxidoreductase from Helicobacter pylori. J. Bacteriol. 177: 3953 3959.
29. Hughes, N. J.,, C. L. Clayton,, P. A. Chalk,, and D. J. Kelly. 1998. Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate:flavodoxin and 2-oxoglutarate:acceptor oxidoreductases which mediate electron transport to NADP. J. Bacteriol. 180: 1119 1128.
30. Jonassen, T.,, and C. F. Clarke,. 2000. Genetic analysis of coenzyme Q biosynthesis, p. 185 208. In P. J. Quinn, and V. E. Kagan (ed.), Coenzyme Q: from Molecular Mechanisms to Nutrition and Health. CRC Press, Boca Raton, Fla..
31. Kather, B.,, K. Stingl,, M. E. vanderRest,, K. Altendorf,, and D. Molenaar. 2000. Another unusual type of citric-acid cycle enzyme in Helicobacter pylori: the malate:quinone oxidoreductase. J. Bacteriol. 182: 3204 3209.
32. Kelly, D. J. 1998. The physiology and metabolism of the human gastric pathogen Helicobacter pylori. Adv. Microb. Physiol. 40: 137 189.
33. Kröger, A.,, V. Geisler,, E. Lemma,, F. Theis,, and R. Lenger. 1992. Bacterial fumarate respiration. Arch. Microbiol. 158: 311 314.
34. Maier, R. J.,, C. Fu,, J. Gilbert,, F. Moshiri,, J. Olson,, and A. G. Plaut. 1996. Hydrogen uptake hydrogenase in Helicobacter pylori. FEMS Microbiol. Lett. 141: 71 76.
35. Marcelli, S. W.,, H.-T., Chang,, T. Chapman,, P. A. Chalk,, R. J. Miles,, and R. K. Poole. 1996. The respiratory chain of Helicobacter pylori: identification of cytochromes and the effects of oxygen on cytochrome and menaquinone levels. FEMS Microbiol. Lett. 138: 59 64.
36. Matin, A.,, E. Zychlinsky,, M. Keyhan,, and G. Sachs. 1996. Capacity of Helicobacter pylori to generate ionic gradients at low pH is similar to that of bacteria which grow under strongly acidic conditions. Infect. Immun. 64: 1434 1436.
37. Mendz, G. L.,, and S. L. Hazell. 1993. Fumarate catabolism in Helicobacter pylori. Biochem. Mol. Biol. Int. 31: 325 332.
38. Mendz, G. L.,, D. J. Meek,, and S. L. Hazell. 1998. Characterisation of fumarate transport in Helicobacter pylori. J. Membrane Biol. 165: 65 76.
39. Meyer-Rosberg, K.,, D. R. Scott,, D. Rex,, K. Melchers,, and G. Sachs. 1996. The effect of environmental pH on the proton-motive force of Helicobacter pylori. Gastroenterology 111: 886 900.
40. Moore, G. R.,, and G. W. Pettigrew. 1990. Cytochromes c. Evolutionary, Structural and Physiochemical Aspects. Springer-Verlag, Berlin, Germany.
41. Moss, C. W.,, M. A. Lambert-Fair,, M. A. Nicholson,, and G. O. Guerrant. 1990. Isoprenoid quinones of Campylobacter cryaerophila, C. cinaedi, C. fennelliae, C. hyointestinalis, C. pylori, and "C. upsaliensis." J. Clin. Microbiol. 28: 395 397.
42. Nagata, K.,, S. Tsukita,, T. Tamura,, and N. Sone. 1996. A cb-type cytochrome-c oxidase terminates the respiratory chain in Helicobacter pylori. Microbiology (U.K.) 142: 1757 1763.
43. Nagata, K.,, H. Yu,, M. Nishikawa,, M. Kashiba,, A. Nakamura,, E. F. Sato,, T. Tamura,, and M. Inouye. 1998. Helicobacter pylori generates superoxide radicals and modulates nitric oxide metabolism. J. Biol. Chem. 273: 14071 14073.
44. Nicholls, D. G.,, and S. J. Ferguson. 1992. Bioenergetics 2. Academic Press Limited, London, United Kingdom.
45. Odenbreit, S.,, B. Wieland,, and R. Haas. 1996. Cloning and genetic characterization of Helicobacter pylori catalase and construction of a catalase-deficient mutant strain, ]. Bacteriol. 178: 6960 6967.
46. 0dum, L.,, and L. P. Andersen. 1995. Investigation of Helicobacter pylori ascorbic acid oxidising activity. FEMS Immunol. Med. Microbiol. 10: 289 294.
47. O'Toole, P. W.,, S. M. Logan,, M. Kostrzynska,, T. Wadström,, and T.J. Trust. 1991. Isolation and biochemical and molecular analyses of a species-specific protein antigen from the gastric pathogen Helicobacter pylori. J. Bacteriol. 173: 505 513.
48. Page, M. D.,, E. Tomlinson,, and S. J. Ferguson. 1997. Unexpected implications from the Helicobacter pylori genome for understanding periplasmic c-type cytochrome assembly in gram-negative bacteria in coexistence with disulphide bond formation. Mol. Microbiol. 26: 413 415.
49. Parkhill, J.,, B. W. Wren,, K. Mungall,, J. M. Ketley,, C. Churcher,, D. Basham,, T. Chillingworth,, R. M. Davies,, T. Felt-well,, S. Holroyd,, K. Jagels,, A. V. Karlyshev,, S. Moule,, M. J. Pallen,, C. W. Penn,, M. A. Quail,, M.-A. Rajandream,, K. M. Rutherford,, A. H. M. van Vliet,, S. Whitehead,, and B. G. Bar-rell. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665 668.
50. Pesci, E. C.,, and C. L. Pickett. 1994. Genetic organisation and enzymatic activity of a superoxoide dismutase from the micro-aerophilic human pathogen, H. pylori. Gene 143: 111 116.
51. Poole, L. B.,, and H. Ellis. 1996. Flavin dependent alkyl hydroperoxide reductase of Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35: 56 64.
52. Poole, R. K.,, and G. M. Cook,. 2000. Redundancy of aerobic respiratory chains in bacteria: routes, reasons and regulation, p. 165 224. In R. K. Poole (ed.), Advances in Microbial Physiology. Academic Press, London, United Kingdom.
53. Poole, R. K.,, and M. N. Hughes. 2000. New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36: 775 783.
54. Smith, M. A.,, and D. L. Edwards. 1997. Oxygen scavenging, NADH oxidase and metronidazole resistance in Helicobacter pylori. J. Antimicrob. Chemother. 39: 347 353.
55. Soballe, B.,, and R. K. Poole. 1999. Microbial ubiquinones: multiple roles in respiration, gene regulation and oxidative stress management. Microbiology 145: 1817 1830.
56. Seballe, B.,, and R. K. Poole. 2000. Ubiquinone limits oxidative stress in Escherichia coli. Microbiology 146: 787 796.
57. Spiegelhalder, C.,, B. Gerstenecker,, A. Kersten,, E. Schiltz,, and M. Kist. 1993. Purification of H. pylori superoxide dismutase and cloning and sequencing of the gene. Infect. Immun. 61: 5315 5325.
58. Storz, G.,, and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2: 188 194.
59. Storz, G.,, F. S. Jacobson,, L. A. Tartaglia,, R. W. Morgan,, L. A. Silveira,, and B. N. Ames. 1989. An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: genetic characterization and cloning of ahp. J. Bacteriol. 171: 2049 2055.
60. Thony-Meyer, L. 1997. Biogenesis of respiratory cytochromes in bacteria. Microbiol. Mol. Biol. Rev. 61: 337 376.
61. Tomb, J.-F.,, O. White,, A. R. Kerlavage,, R. A. Clayton,, G. G. Sutton,, R. D. Fleishmann,, K. A. Ketchum,, H. P. Klenk,, S. Gill,, B. Dougherty,, K. Nelson,, J. Quackenbush,, L. Zhou,, E. F. Kirkness,, S. Peterson,, B. Loftus,, D. Richardson,, R. Dodson,, H. G. Khalak,, A. Glodek,, K. McKenney,, L. M. Fitzegerald,, N. Lee,, M. D. Adams,, E. Hickey,, D. E. Berg,, J. D. Gocayne,, T. R. Utterback,, J. D. Peterson,, J. M. Kelley,, M. D. Cotton,, J. M. Weidman,, C. Fujii,, C. Bowman,, L. Watthey,, E. Wallin,, W. S. Hayes,, M. Borodovsky,, P. D. Karp,, H. O. Smith,, C. M. Fraser,, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539 547.
62. Tsukita, S.,, S. Koyanagi,, K. Nagata,, H. Koizuka,, H. Akashi,, T. Shimoyama,, T. Tamura,, and N. Sone. 1999. Characterisation of a cb-type cytochrome c oxidase from Helicobacter pylori. ]. Biochem. 125: 194 201.
63. Tuckwell, A.,, and P. A. Chalk. 1993. Factors affecting the survival of liquid cultures of Helicobacter pylori in air. Acta Gastro-Enterol. Belg. 56S: 101.
64. van Vliet, A. H. M.,, M. L. A. Baillon,, C. Penn,, and J. M. Ketley. 1999. Campylobacter jejuni contains two Fur homologues: characterisation of iron-responsive regulation of peroxide stress defense genes by the PerR repressor, J. Bacteriol. 181: 6371 6376.
65. Wan, X.,, Y. Zhou,, Z. Yan,, H. Wang,, Y. Hou,, and D. Jin. 1997. Scavengase p20: a novel family of bacterial antioxidant enzymes. FEBS Lett. 407: 32 36.

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