Complexity and Versatility in the Physiology and Metabolism of Campylobacter jejuni

David J. Kelly

doi:10.1128/9781555815554.ch3

Chapter 3 : Complexity and Versatility in the Physiology and Metabolism of Campylobacter jejuni

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Molecular Biology and Biotechnology, University of Sheffield, Firth Court, Western Bank, Sheffield S10 2TN, United Kingdom

Content Type: Monograph

Publication Year: 2008

Category: Bacterial Pathogenesis

Book DOI: 10.1128/9781555815554

Chapter DOI: 10.1128/9781555815554.ch3

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Complexity and Versatility in the Physiology and Metabolism of Campylobacter jejuni, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap03-1.gif /docserver/preview/fulltext/10.1128/9781555815554/9781555814373_Chap03-2.gif

Abstract:

This chapter reviews the current knowledge on some of the metabolic aspects of Campylobacter jejuni physiology, with emphasis on those features of carbon, nitrogen, and electron flow that are likely to be of importance in understanding growth in the environment and in vivo. It focuses on catabolic pathways, i.e., those involved in the breakdown of extracellular solutes, yielding energy and key intracellular intermediates that are the building blocks for new cell growth. It describes the transport systems that relate to the major metabolic pathways in C. jejuni for which some functional data are available. C4-dicarboxylate transport (malate, succinate, fumarate, and possibly also aspartate) seems to be particularly important in C. jejuni. These substrates can feed directly into the citric acid cycle (CAC), malate and succinate can act as direct electron donors for aerobic respiration, and fumarate is an alternative electron acceptor under oxygen-limiting conditions. The chapter also focuses on central carbon metabolism in C. jejuni, and amino acid catabolism and nitrogen assimilation. A variety of primary dehydrogenases can be identified that feed electrons to a menaquinone pool. C. jejuni contains a proton-translocating cytochrome bc 1 complex feeding electrons to a periplasmic c-type cytochrome (probably Cj1153 in NCTC 11168) and then to a high-affinity cb-type oxidase, which allows efficient energy conservation when oxygen is used as electron acceptor. One conclusion that can be drawn is that many campylobacters show an unexpected metabolic versatility, which is particularly reflected in the complexity of the electron transport chains in C. jejuni.

Citation: Kelly D. 2008. Complexity and Versatility in the Physiology and Metabolism of Campylobacter jejuni, p 41-61. In Nachamkin I, Szymanski C, Blaser M (ed), Campylobacter, Third Edition. ASM Press, Washington, DC. doi: 10.1128/9781555815554.ch3

Key Concept Ranking

Aromatic Amino Acids: 0.50511444
Major Facilitator Superfamily: 0.5035242
Multienzyme Complex: 0.4539895
Electron Transport System: 0.43080765

0.50511444

Highlighted Text: Show | Hide

Full text loading...

Figures

Complexity and Versatility in the Physiology and Metabolism of Campylobacter jejuni

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555815554.ch03-1,webId=/content/author/10.1128/9781555815554.ch03-1,properties={foaf_givenname=David J., foaf_name=David J. Kelly, foaf_surname=Kelly, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555815554.ch03-aff1]]}]]

/content/10.1128/9781555815554.ch03.ch03fig01

Figure 1.

Major pathways of central carbon metabolism and amino acid utilization in C. jejuni. The cell is represented with an outer membrane (OM) and inner membrane (IM), enclosing the periplasm, and a cytoplasm within which the major pathways of carbon metabolism are shown. Key amino acid transport systems are shown as black rectangles in the inner membrane. The black circle emphasizes the transamination reaction that converts glutamate to aspartate. The major enzymes are shown next to the reactions catalyzed. SdaC, serine transporter; SdaA, serine dehydratase; Pyk, pyruvate kinase; Pyc, pyruvate carboxylase; Pck, PEP carboxykinase; Por, pyruvate:acceptor oxidoreductase; Acs, acetyl-CoA synthetase; Pta, phosphotransacetylase; AckA, acetate kinase; GltA, citrate synthase; Acn, aconitase; Icd, isocitrate dehydrogenase; Oor, 2-oxoglutarate:acceptor oxidoreductase; Suc, succinyl-CoA synthetase; Sdh, succinate dehydrogenase; Fum, fumarase; Mqo, malate:quinone oxidoreductase; Mdh, malate dehydrogenase (NAD linked); AspA, aspartase; Aat, aspartate:glutamate amino-transferase; GlnA, glutamine synthase; GltBD, glutamate synthase; PutA, proline dehydrogenase; PutP, proline transporter; GGT, γ-glutamyl transpeptidase. The conversion of glutathione to glutamate ocurrs in the periplasm of some strains only (dotted arrow). The Peb1 system is an ABC transporter containing the periplasmic aspartate/glutamate binding protein Peb1a. Fld, flavodoxin; Fd, ferredoxin. OAA, oxaloacetate; PEP, phosphoenol pyruvate; AcP, acetyl-phosphate.

10.1128/9781555815554/f0045-01_thmb.gif

10.1128/9781555815554/f0045-01.gif

Figure 1.

/content/10.1128/9781555815554.ch03.ch03fig02

Figure 2.

Major electron transport pathways in C. jejuni. Integral membrane oxidoreductases on the electron donor side of the menaquinone (MK) pool include an NDH-1-like complex (Cj1566–1579), the electron donor to which is unknown, hydrogenase, formate dehydrogenase, and succinate dehydrogenase. Peripherally associated oxidoreductases include (among several others) malate:quinone oxidoreductase, proline dehydrogenase, and a lactate dehydrogenase. Reducing equivalents are transferred to menaquinone in the lipid bilayer of the inner membrane. Menaquinol reduces the cytochrome bc 1 complex, which in turn reduces periplasmic cytochrome c. Cytochrome c is reoxidized by one of the terminal oxidases, a cb-type cytochrome c oxidase. A separate quinol oxidase (CioAB) is also present. Cytochrome c may also be reoxidized by hydrogen peroxide in the periplasm through the activity of two separate CCPs. Several alternative reductases are present in C. jejuni. Fumarate reductase (FrdCAB) catalyzes electron transfer from menaquinol to fumarate as terminal acceptor. Periplasmic nitrate (Nap), nitrite (Nrf), and TMAO/DMSO reductases (Tor/Dor) are also present. An additional type of DMSO reductase (DmsABC) is present in strain 81-176 (not shown; see text and Fig. 3 for details). Cj0378/379 are homologues of the E. coli YedZ/YedY proteins, which are a b-type cytochrome and a molybdoprotein reductase, respectively, but the substrate reduced is unknown. Solid lines indicate experimentally established or highly likely routes of electron transport; dotted lines indicate uncertainty as to the exact route, possibly with the participation of unidentified additional redox proteins. Figure modified and updated from Kelly (2005) .

10.1128/9781555815554/f0048-01_thmb.gif

10.1128/9781555815554/f0048-01.gif

Figure 2.

/content/10.1128/9781555815554.ch03.ch03fig03

Figure 3.

Likely topological organization of two types of TMAO/DMSO reductases found in strains of C. jejuni. In each case, formate is depicted as a typical electron donor to the menaquinone pool (MK), through the action of formate dehydrogenase (Fdh). (a) The Tor/Dor type of reductase system that has been characterized in strain 11168 ( Sellars et al., 2002 ) is illustrated, which is also present in strains RM1221 and 81-176. There is uncertainty over the mechanism of electron transfer from the MK to the monoheme Cj0265 cytochrome (dashed rectangular hypothetical quinol oxidoreductase). In (b), the additional DmsABC-type system shown in strain 81-176 to be needed for optimal colonization of a mouse infection model ( Hofreuter et al., 2006 ) is illustrated. Note that because both of these TMAO/DMSO reductases are predicted to be periplasmic, reduction of the electron acceptor (which consumes protons—in bold) and quinol oxidation (which releases protons—in bold) occur on the same (periplasmic) side of the membrane. Thus, a proton-motive force is only generated at the level of the primary dehydrogenase (binding and releasing protons on opposite sides of the membrane). MGD, molybdenum guanosine dinucleoside cofactor.

10.1128/9781555815554/f0057-01_thmb.gif

10.1128/9781555815554/f0057-01.gif

Figure 3.

References

/content/book/10.1128/9781555815554.ch03

1. Atack, J. M., and, D. J. Kelly. 2007. Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases. Adv. Microb. Physiol. 52: 73– 106.

2. Baltes, N.,, I. Hennig-Pauka,, I. Jacobsen,, A. D. Gruber, and, G. F. Gerlach. 2003. Identification of dimethyl sulphoxide reductase in Actinobacillus pleuropneumoniae and its role in infection. Infect. Immun. 71: 6784– 6792.

3. Barnes, H. A.,, M. C. Bagnall.,, D. D. Browning,, S. A. Thompson,, G. Manning, and, D. G. Newell. 2007. γ-Glutamayl transpeptidase has a role in persistent colonisation of the avian gut by Campylobacter jejuni. Microb. Pathog. 43: 198– 207.

4. Berg, B. L.,, J. Li,, J. Heider, and, V. Stewart. 1991. Nitrateinducible formate dehydrogenase in Escherichia coli K-12. I. Nucletide sequence of the fdnGHI operon and evidence that opal (UGA) encodes selenocysteine. J. Biol. Chem. 266: 22380– 22385.

5. Bras, A. M.,, S. Chatterjee,, B. W. Wren,, D. G. Newell and, J. M. Ketley. 1999. A novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J. Bacteriol. 181: 3298– 3302.

6. Brondijk, T. H. C.,, D. Fiegen,, D. J. Richardson, and, J. A. Cole. 2002. Roles of NapF, NapG, and NapH, subunits of the Escherichia coli periplasmic nitrate reductase, in ubiquinol oxidation. Mol. Microbiol. 44: 245– 255.

7. Brondijk, T. H. C.,, A. Nilavongse,, N. Filenko,, D. J. Richardson, and, J. A. Cole. 2004. NapGH components of the periplasmic nitrate reductase of Escherichia coli K-12: location, topology, and physiological roles in quinol oxidation and redox balancing. Biochem. J. 379: 47– 55.

8. Carlone, G. M., and, J. Lascelles, J. 1982. Aerobic and anaerobic respiratory systems in Campylobacter fetus subsp. jejuni grown in atmospheres containing hydrogen. J. Bacteriol. 152: 306– 314.

9. Chang, D. E.,, D. J. Smalley,, D. L. Tucker,, M. P. Leatham,, W. E. Norris,, S. J. Stevenson,, A. B. Anderson,, J. E. Grissom,, D. C. Laux,, P. S. Cohen, and, T. Conway. 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Natl. Acad. Sci. USA 101: 7427– 7432.

10. Costa, C.,, A. Macedo,, I. Moura,, J. Moura,, J. LeGall,, Y. Berlier,, M. Y. Liu, and, W. Payne. 1990. Regulation of the hexa-heme nitrite: nitric oxide reductase of Desulfovibrio desulfuricans, Wolinella succinogenes, and Escherichia coli: a mass spectrometric study. FEBS Lett. 276: 67– 70.

11. Daucher, J. A., and, N. R. Kreig. 1995. Pyruvate-ferredoxin oxidoreductase in Campylobacter species. Can. J. Microbiol. 41: 198– 201.

12. Einsle, O.,, P. Stach,, A. Messerschmidt,, J. Simon,, A. Kröger,, R. Huber, and, M. H. Kroneck. 2000. Cytochrome c nitrite reductase from Wolinella succinogenes. J. Biol. Chem. 275: 39608– 39616.

13. Elvers, K. T.,, S. M. Turner,, L. M. Wainwright,, G. Marsden,, J. Hinds,, J. A. Cole,, R. K. Poole,, C. W. Penn, and, S. F. Park. 2005. NssR, a member of the Crp-Fnr superfamily from Campylobacter jejuni, regulates a nitrosative stress-responsive regulon that includes both a single-domain and a truncated haemoglobin. Mol. Microbiol. 57: 735– 750.

14. Elvers, K. T.,, G. Wu,, N. J. Gilberthorpe,, R. K. Poole, and, S. F. Park. 2004. Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Camplylobacter jejuni and Campylobacter coli. J. Bacteriol. 186: 5332– 5341.

15. Finel, M. 1998. Does NADH play a central role in energy metabolism in Helicobacter pylori? Trends Biochem. Sci. 23: 412– 414.

16. Fouts, D. E.,, E. F. Mongodin,, R. E. Mandrell,, W. G. Miller,, D. A. Rasko,, J. Ravel,, L. M. Brinkac,, R. T. DeBoy,, C. T. Parker,, S. C. Daugherty,, R. J. Dodson,, A. Scott-Durkin,, R. Madupu,, S. A. Sullivan,, J. U. Shetty,, M. A. Ayodeji,, A. Shvartsbeyn,, M. C. Schatz,, J. H. Badger,, C. M. Fraser, and, K. E. Nelson. 2005. Major structural differences and novel potential virulence mechanisms form the genomes of multiple Campylobacter species. PLoS Biol. 3: 72– 85.

17. Gaynor, E. C.,, S. Cawthraw,, G. Manning,, J. K. MacKichan,, S. Falkow, and, D. G. Newell. 2004. The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J. Bacteriol. 186: 503– 517.

18. Godlewska, R.,, M. Pawowski,, A. Wyszynska,, J. Bujnicki, and, E. Jagusztyn-Krynicka. 2005. Sorting of Campylobacter jejuni lipoproteins, abstr. F17, p. 82. Abstr. 13th Int. Workshop Campylobacter Helicobacter Relat. Organisms, Gold Coast, Australia, 4 to 8 September 2005.

19. Gon, S.,, M. T. Guidici-Orticoni,, V. Mejean, and, C. Iobbi-Nivol. 2001. Electron transfer and binding of the c-type cytochrome TorC to the trimethylamine N-oxide reductase in Escherichia coli. J. Biol. Chem. 276: 11545– 11551.

20. Goodhew, C. F.,, A. B. ElKurdi, and, G. W. Pettigrew. 1988. The microaerophilic respiration of Campylobacter mucosalis. Biochim. Biophys. Acta 933: 114– 123.

21. Goss, J. A.,, N. D. Cohen, N. D., and, M. F. Utter. 1981. Characterisation of the subunit structure of pyruvate carboxylase from Pseudomonas citronellolis. J. Biol. Chem. 256: 11819– 11825.

22. Grabowski, R., A., E. M. Hofmeister, and, W. Buckel. 1993. Bacterial l-serine dehydratases: a new family of enzymes containing iron-sulfur clusters. Trends Biochem. Sci. 18: 297– 300.

23. Hama, H.,, T. Shimamoto,, M. Tsuda, and, T. Tsuchiya. 1987. Properties of a Na +-coupled serine-threonine transport system in Escherichia coli. Biochim. Biophys. Acta. 905: 231– 239.

24. Hendrixson, D. R., and, V. J. DiRita. 2004. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52: 471– 484.

25. Hinton, A. 2006. Growth of Campylobacter in media supplemented with organic acids. J. Food Prot. 69: 34– 38.

26. Hoffman, P. S., and, T. G. Goodman. 1982. Respiratory physiology and energy conservation efficiency of Campylobacter jejuni. J. Bacteriol. 150: 319– 326.

27. Hofreuter, D.,, J. Tsai,, R. O. Watson,, V. Novik,, B. Altman,, M. Benitez,, C. Clark,, C. Perbost,, T. Jarvie,, L. Du, and, J. E. Galan. 2006. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74: 4694– 4707.

28. Holmes, K.,, F. Mulholland,, B. M. Pearson,, C. Pin,, J. McNicholl-Kennedy,, J. M. Ketley, and, J. M. Wells. 2005. Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151: 243– 257.

29. Huang, J., and, M. A. Schell. 1992. Role of the two-component leader sequence and mature amino-acid sequences in extracellular export of endoglucanase EGL from Pseudomonas solanacearum. J. Bacteriol. 174: 1314– 1323.

30. 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.

31. 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.

32. Jackson, R. J.,, K. T. Elvers,, L. J. Lee,, M. D. Gidley,, L. M. Wainwright,, J. Lightfoot,, S. F. Park, and, R. K. Poole. 2007. Oxygen reactivity of both respiratory oxidases in Campylobacter jejuni: the cydAB genes encode a cyanide-resistant, low-affinity oxidase that is not of the cytochrome bd type. J. Bacteriol. 189: 1604– 1615.

33. Kanamori, T.,, K, Norihisa,, H. Atomi, and, T. Imanaka. 2004. Enzymatic characterisation of a prokaryotic urea carboxylase. J. Bacteriol. 186: 2532– 2539.

34. Karmali, M. A.,, M. Roscoe, and, P. C. Fleming. 1986. Modified ammonia electrode method to investigate d-asparagine breakdown by Campylobacter strains. J. Clin. Microbiol. 23: 743– 747.

35. Kather, B.,, K. Stingl,, M. E. van der Rest,, K. Altendorf, and, D. Molenaar. 2000. Another unusual type of citric acid cycle enzyme in Helicobacter pylori: malate:quinone oxidoreductase. J. Bacteriol. 182: 3204– 3209.

36. Kelly, D. J. 1998. The physiology and metabolism of the human gastric pathogen Helicobacter pylori. Adv. Microb. Physiol. 40: 137– 189.

37. Kelly, D. J. 2001. The physiology and metabolism of Campylobacter jejuni and Helicobacter pylori. J. Appl. Microbiol. 90: 16S– 24S.

38. Kelly, D. J. 2005. Metabolism, electron transport and bioenergetics of Campylobacter jejuni: implications for understanding life in the gut and survival in the environment, p. 275– 292. In J. M. Ketley and, M. E. Konkel (ed.), Campylobacter jejuni: Molecular and Cellular Biology. Horizon Press, Wymondham, United Kingdom.

39. Kelly, D. J.,, N. J. Hughes, N. J., and, R. K. Poole. 2001. Microaerobic physiology: aerobic respiration, anaerobic respiration, and carbon dioxide metabolism, p. 113– 124. In H. L. T. Mobley,, G. L. Mendz, and, S. L. Hazell (ed.), Helicobacter pylori: Physiology and Genetics. ASM Press, Washington, DC.

40. Kreig, N. R. and, P. S. Hoffman. 1986. Microaerophily and oxygen toxicity. Ann. Rev. Microbiol. 40: 107– 130.

41. Kröger, A.,, S. Biel.,, J. Simon,, R. Gross,, G. Unden, and, C. R. Lancaster. 2002. Fumarate respiration of Wolinella succinogenes: enzymology, energetics and coupling mechanism. Biochim. Biophys. Acta 1553: 23– 38.

42. Lancaster, C. R. D. 2002. Wolinella succinogenes quinol: fumarate reductase-2.2 Å resolution crystal structure and the E-pathway hypothesis of coupled transmembrane proton and electron transfer. Biochim. Biophys. Acta 1565: 215– 231.

43. Leach, S.,, P. Harvey, and, R. Wait. 1997. Changes with growth rate in the membrane lipid composition of and amino-acid utilisation by continuous cultures of Campylobacter jejuni. J. Appl. Microbiol. 82: 631– 640.

44. Lee, Y.,, D. H. Lee,, C. W. Kho.,, A. Y. Lee,, M. Jang.,, S. Cho,, C. H. Lee,, J. S. Lee,, P. K. Myung,, B. C. Park, and, S. G. Park. 2005. Transthyretin-related proteins function to facilitate the hydrolysis of 5-hydroxyisourate, the end product of the uricase reaction. FEBS Lett. 579: 4769– 4774.

45. Leon-Kempis, M del R.,, E. Guccione,, F. Mulholland,, M. P. Williamson, and, D. J. Kelly. 2006. The Campylobacter jejuni PEB1a adhesin is an aspartate/glutamate-binding protein of an ABC transporter essential for microaerobic growth on dicarboxylic amino acids. Mol. Microbiol. 60: 1262– 1275.

46. Loschi, L.,, S. J. Brokx,, T. L. Hills,, G. Zhang,, M. G. Botero,, A. L. Lovering,, J. H. Weiner, and, N. C. Strynadka. 2004. Structural and biochemical identification of a novel bacterial oxidoreductase. J. Biol. Chem. 279: 50391– 503400.

47. Marceau, M.,, S. D. Lewis, and, J. A. Shafer. 1988. The glycine-rich region of Escherichia coli d-serine dehydratase. Altered interaction with pyridoxal 5′-phosphate produced by substitution of aspartic acid for glycine. J. Biol. Chem. 263: 16934– 16941.

48. McCrindle, S. L.,, U. Kappler and, A. G. McEwan. 2005. Microbial dimethylsulfoxide and trimethylamine-N-oxide respiration. Adv. Microb. Phys. 50: 147– 198.

49. Mendz, G. L.,, G. E. Ball, and, D. J. Meek. 1997. Pyruvate metabolism in Campylobacter spp. Biochim. Biophys. Acta. 1334: 291– 302.

50. Müller, A.,, M. del, R. Leon-Kempis,, E. Dodson,, K. S. Wilson,, A. J. Wilkinson, and, D. J. Kelly. 2007. A bacterial virulence factor with a dual role as an adhesin and a solute-binding protein: the crystal structure at 1.5 Å resolution of the PEB1a protein from the food-borne human pathogen Campylobacter jejuni. J. Mol. Biol. 372: 160– 171.

51. Müller, A.,, G. H. Thomas,, R. Horler,, J. A. Brannigan,, E. Blagova,, V. M. Levdikov,, M. J. Fogg,, K. S. Wilson, and, A. J. Wilkinson. 2005. An ATP-binding cassette-type cysteine transporter in Campylobacter jejuni inferred from the structure of an extra-cytoplasmic solute receptor protein. Mol. Microbiol. 57: 143– 155.

52. Myers, J. D., and, D. J. Kelly. 2005. A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology 151: 233– 242.

53. Nagata, K.,, S. Tsukita,, T. Tamura and, N. Sone. 1996. A cb-type cytochrome- c oxidase terminates the respiratory chain in Helicobacter pylori. Microbiology 142: 1757– 1763.

54. Ogawa, H.,, K. Konishi, K., and, M. Fujioka. 1989. The peptide sequences near the bound pyridoxal phosphate are conserved in serine dehydratase from rat liver and threonine dehydratases from yeast and Escherichia coli. Biochim. Biophys. Acta. 139: 139– 141.

55. Olson, J. W., and, R. J. Maier. 2002. Molecular hydrogen as an energy source for Helicobacter pylori. Science 298: 1788– 1790.

56. Palmer, T.,, F. Sargent, and, B. C. Berks. 2005. Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol. 13: 175– 180.

57. Parkhill, J.,, B. W. Wren,, K. Mungall,, J. M. Ketley,, C. Churcher,, D. Basham,, T. Chillingworth,, R. M. Davies,, T. Feltwell,, 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. Barrell. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665– 668.

58. Parsons, C. M.,, L. M. Potter, and, R. D. Brown Jr. 1982. Effects of dietary protein and intestinal microflora on excretion of amino-acids in poultry. Poult. Sci. 61: 939– 946.

59. Pei, Z., and, M. J. Blaser. 1993. PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in gram-negative nutrient transport systems. J. Biol. Chem. 268: 18717– 18725.

60. Pei, Z.,, C. Burucoa,, B. Grignon,, S. Baqar,, X. Z. Huang,, D. J. Kopecko,, A. L. Bourgeois,, J. L. Fauchere, and, M. J. Blaser. 1998. Mutation in the peb1A locus of Campylobacter jejuni reduces interactions with epithelial cells and intestinal colonization of mice. Infect. Immun. 66: 938– 943.

61. Pei, Z. H.,, R. T. Ellison III, and, M. J. Blaser. 1991. Identification, purification, and characterization of major antigenic proteins of Campylobacter jejuni. J. Biol. Chem. 266: 16363– 16369.

62. Pisa, R.,, T. Stein,, R. Eichler,, R. Gross, and, J. Simon. 2002. The nrfI gene is essential for the attachment of the active site haem group of Wolinella succinogenes cytochrome c nitrite reductase. Mol. Microbiol. 43: 763– 770.

63. Pittman, M. S.,, K. T. Elvers,, L. Lee,, M. Jones,, R. K. Poole,, S. F. Park, and, D. J. Kelly. 2007. Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via an atypical NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol. Microbiol. 63: 575– 590.

64. Poly, F.,, T. Read.,, D. R. Tribble,, S. Baqar,, M. Loenzo, and, P. Guerry. 2007. Genome sequence of a clinical isolate of Campylobacter jejuni from Thailand. Infect. Immun. 75: 3425– 3433.

65. Poock, S. R.,, E. R. Leach,, J. W. B. Moir,, J. A. Cole, and, D. J. Richardson. 2002. Respiratory detoxification of nitric oxide by the cytochrome c nitrite reductase of Escherichia coli. J. Biol. Chem. 277: 23664– 23669.

66. Poole, R. K., and, G. M. Cook. 2000. Redundancy of aerobic respiratory chains in bacteria: routes, reasons and regulation. Adv. Microb. Physiol. 42: 165– 224.

67. Seaver, L. C., and, J. A. Imlay. 2004. Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J. Biol. Chem. 279: 48742– 48750.

68. Sellars, M. J.,, S. J. Hall, and, D. J. Kelly. 2002. Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide or dimethylsulfoxide requires oxygen. J. Bacteriol. 184: 4187– 4196.

69. Shibayama, K.,, J-I. Wachino,, Y. Arakawa,, M. Saidijam,, N. G. Rutherford, and, P. J. F. Henderson. 2007. Metabolism of glutamine and glutathione via γ-glutamyl transpeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol. Microbiol. 64: 396– 406.

70. Simon, J. 2002. Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol. Rev. 26: 285– 309.

71. Simon, J.,, R. Gross,, O. Einsle,, P. M. H. Kroneck,, A. Kröger, and, O. Klimmek. 2000. A NapC/NirT-type cytochrome c (NrfH) is the mediator between the quinone pool and the cytochrome c nitrite reductase of Wolinella succinogenes. Mol. Microbiol. 35: 686– 696.

72. Simon J.,, M. Sanger,, S. C. Schuster, and, R. Gross. 2003. Electron transport to the periplasmic nitrate reductase (NapA) of Wolinella succinogenes is independent of a NapC protein. Mol. Microbiol. 49: 69– 79.

73. Smith, M. A.,, M. Finel,, V. Korolik, and, G. L. Mendz. 2000. Characteristics of the aerobic respiratory chains of the microaerophiles Campylobacter jejuni and Helicobacter pylori. Arch. Microbiol. 174: 1– 10.

74. St Maurice, M.,, N. Cremades,, M. A. Croxen,, G. Sisson,, J. Sancho, and, P. S. Hoffman. 2007. Flavodoxin:quinone reductase (FqrB): a redox partner of pyruvate:ferredoxin oxidoreductase that reversibly couples pyruvate oxidation to NADPH production in Helicobacter pylori and Campylobacter jejuni. J. Bacteriol. 189: 4764– 4773.

75. Unden, G., and, A. Kleefeld. 2004. Chapter 3.4.5. C 4-dicarboxylate degradation in aerobic and anaerobic growth. In R. Curtiss III et al. (ed.), EcoSal—Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, DC. http://www.ecosal.org/.

76. Velayudhan, J.,, M. A. Jones,, P. A. Barrow, and, D. J. Kelly. 2004. l-Serine catabolism via an oxygen-labile l-serine dehydratase (SdaA) is essential for colonisation of the avian gut by Campylobacter jejuni. Infect. Immun. 72: 260– 268.

77. Velayudhan, J., and, D. J. Kelly. 2002. Analysis of gluconeogenic and anaplerotic enzymes in Campylobacter jejuni: an essential role for phosphoenolpyruvate carboxykinase. Microbiology. 148: 685– 694.

78. Weber, I.,, C. Fritz,, S. Ruttkowski,, A. Kreft, and, F. C. Bange. 2000. Anaerobic nitrate reductase ( narGHJI) activity of Mycobacterium bovis BCG in vitro and its contribution to virulence in immunodeficient mice. Mol. Microbiol. 35: 1017– 1025.

79. Westfall, H. N.,, D. M. Rollins, and, E. Weiss. 1986. Substrate utilisation by Campylobacter jejuni and Campylobacter coli. Appl. Environ. Microbiol. 52: 700– 705.

80. Woodall, C. A.,, M. A. Jones,, P. A. Barrow,, J. Hinds,, G. L. Mars-den,, D. J. Kelly,, N. Dorrell,, B. W. Wren, and, D. J. Maskell. 2005. Campylobacter jejuni gene expression in the chick cecum: evidence for adaptation to a low-oxygen environment. Infect. Immun. 73: 5278– 5285.

81. Wyszynska, A.,, M. Pawlowski,, J. Bujnicki,, D. Pawelec.,, J. P. van Putten.,, E. Brzuszkiewicz, and, E. K. Jagusztyn-Krynicka. 2006. Genetic characterisation of the cjaAB operon of Campylobacter coli. Pol. J. Microbiol. 55: 85– 94.