Anaerobic respiration of fumarate as a differential test betweenCampylobacter fetus andCampylobacter jejuni

Véron, Michel; Lenvoisé-Furet, Annie; Beaune, Philippe

doi:10.1007/bf01567010

Cited by 21 publications

(15 citation statements)

References 17 publications

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“…It has previously been reported that C. jejuni is incapable of anaerobic growth with fumarate as the electron acceptor (28). However, the presence of fumarate reductase activity (4, 26) encoded by typical frd genes distinct from those encoding succinate dehydrogenase (12,19) suggests that anaerobic growth supported by fumarate respiration might be possible.…”

Section: Resultsmentioning

confidence: 99%

“…Early research on respiration in campylobacters led to the realization that some species, e.g., Campylobacter fetus (28), could grow anaerobically by using fumarate as an electron acceptor, but this capacity was reported as being absent from C. jejuni (28). In this study, we have obtained clear evidence that C. jejuni is capable of growth that is supported by respiration of a range of electron acceptors, including fumarate, nitrate, nitrite, and TMAO or DMSO.…”

Section: Discussionmentioning

confidence: 99%

“…ent only in cultures in which growth is limited by a reduced oxygen supply but which are not anaerobic. This requirement for oxygen accounts for the inability of previous investigators to obtain the growth of C. jejuni under strictly anaerobic conditions (28). Although other oxygen-requiring processes could contribute to the prevention of anaerobic growth, the most likely essential role of oxygen is to satisfy the requirement for deoxyribonucleotide in DNA synthesis due to the use of an oxygen-utilizing class I-type RNR.…”

Section: Discussionmentioning

confidence: 99%

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Growth ofCampylobacter jejuniSupported by Respiration of Fumarate, Nitrate, Nitrite, Trimethylamine-N-Oxide, or Dimethyl Sulfoxide Requires Oxygen

2002

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The human gastrointestinal pathogen Campylobacter jejuni is a microaerophilic bacterium with a respiratory metabolism. The genome sequence of C. jejuni strain 11168 reveals the presence of genes that encode terminal reductases that are predicted to allow the use of a wide range of alternative electron acceptors to oxygen, including fumarate, nitrate, nitrite, and N-or S-oxides. All of these reductase activities were present in cells of strain 11168, and the molybdoenzyme encoded by Cj0264c was shown by mutagenesis to be responsible for both trimethylamine-N-oxide (TMAO) and dimethyl sulfoxide (DMSO) reduction. Nevertheless, growth of C. jejuni under strictly anaerobic conditions (with hydrogen or formate as electron donor) in the presence of any of the electron acceptors tested was insignificant. However, when fumarate, nitrate, nitrite, TMAO, or DMSO was added to microaerobic cultures in which the rate of oxygen transfer was severely restricted, clear increases in both the growth rate and final cell density compared to what was seen with the control were obtained, indicative of electron acceptor-dependent energy conservation. The C. jejuni genome encodes a single class I-type ribonucleotide reductase (RNR) which requires oxygen to generate a tyrosyl radical for catalysis. Electron microscopy of cells that had been incubated under strictly anaerobic conditions with an electron acceptor showed filamentation due to an inhibition of cell division similar to that induced by the RNR inhibitor hydroxyurea. An oxygen requirement for DNA synthesis can thus explain the lack of anaerobic growth of C. jejuni. The results indicate that strict anaerobiosis is a stress condition for C. jejuni but that alternative respiratory pathways can contribute significantly to energy conservation under oxygen-limited conditions, as might be found in vivo.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Growth ofCampylobacter jejuniSupported by Respiration of Fumarate, Nitrate, Nitrite, Trimethylamine-N-Oxide, or Dimethyl Sulfoxide Requires Oxygen

2002

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“…Mutations in this enzyme have serious and previously unsuspected implications for the growth and metabolic flexibility of this important pathogen. Although fumarate reductase activity has been measured in C. jejuni (37,38), this organism is unable to respire anaerobically using fumarate as a terminal electron acceptor (37,41), leaving the physiological role of the fumarate reductase in doubt. We constructed mutants with mutations in both the fumarate reductase and succinate dehydrogenase in order determine the in vivo functions of these two enzymes.…”

Section: Discussionmentioning

confidence: 99%

“…Fumarate reductase (Frd) activity has been reported to occur in the particulate fraction of C. jejuni cell lysates, and addition of formate to whole cells increased Frd activity (38), which implies that there is an active electron transport pathway. However, C. jejuni is unable to utilize fumarate as an alternative electron acceptor under anaerobic conditions (37,41). C. jejuni can also use succinate as an electron donor to a respiratory quinone (12), which has been identified as either a menaquinone-6 or methylmenaquinone-6 (4).…”

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The Dual-Functioning Fumarate Reductase Is the Sole Succinate:Quinone Reductase in Campylobacter jejuni and Is Required for Full Host Colonization

2009

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Campylobacter jejuni encodes all the enzymes necessary for a complete oxidative tricarboxylic acid (TCA) cycle. Because of its inability to utilize glucose, C. jejuni relies exclusively on amino acids as the source of reduced carbon, and they are incorporated into central carbon metabolism. The oxidation of succinate to fumarate is a key step in the oxidative TCA cycle. C. jejuni encodes enzymes annotated as a fumarate reductase (Cj0408 to Cj0410) and a succinate dehydrogenase (Cj0437 to Cj0439). Null alleles in the genes encoding each enzyme were constructed. Both enzymes contributed to the total fumarate reductase activity in vitro. The frdA::cat ؉ strain was completely deficient in succinate dehydrogenase activity in vitro and was unable to perform whole-cell succinate-dependent respiration. The sdhA::cat ؉ strain exhibited wild-type levels of succinate dehydrogenase activity both in vivo and in vitro. These data indicate that Frd is the only succinate dehydrogenase in C. jejuni and that the protein annotated as a succinate dehydrogenase has been misannotated. The frdA::cat ؉ strain was also unable to grow with the characteristic wild-type biphasic growth pattern and exhibited only the first growth phase, which is marked by the consumption of aspartate, serine, and associated organic acids. Substrates consumed in the second growth phase (glutamate, proline, and associated organic acids) were not catabolized by the the frdA::cat ؉ strain, indicating that the oxidation of succinate is a crucial step in metabolism of these substrates. Chicken colonization trials confirmed the in vivo importance of succinate oxidation, as the frdA::cat ؉ strain colonized chickens at significantly lower levels than the wild type, while the sdhA::cat ؉ strain colonized chickens at wild-type levels.

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CampylobacterandArcobacter

Vandenberg

Skirrow

Butzler

2010

Topley &Amp; Wilson's Microbiology and Microbial Infections

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Anaerobic respiration of fumarate as a differential test betweenCampylobacter fetus andCampylobacter jejuni

Cited by 21 publications

References 17 publications

Growth ofCampylobacter jejuniSupported by Respiration of Fumarate, Nitrate, Nitrite, Trimethylamine-N-Oxide, or Dimethyl Sulfoxide Requires Oxygen

Growth ofCampylobacter jejuniSupported by Respiration of Fumarate, Nitrate, Nitrite, Trimethylamine-N-Oxide, or Dimethyl Sulfoxide Requires Oxygen

The Dual-Functioning Fumarate Reductase Is the Sole Succinate:Quinone Reductase in Campylobacter jejuni and Is Required for Full Host Colonization

CampylobacterandArcobacter

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