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

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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

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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

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Complexity and Versatility in the Physiology and Metabolism of Campylobacter jejuni

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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.

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Figure 1.

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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) .

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Figure 2.

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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.

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Figure 3.

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