A temperature-regulated Campylobacter jejuni gluconate dehydrogenase is involved in respiration-dependent energy conservation and chicken colonization

Mohanasundari Pajaniappan, Johanna E. Hall, Shaun A. Cawthraw, Diane G. Newell, Erin C. Gaynor, Joshua A. Fields, Kimberly M. Rathbun, Willie A. Agee, Christopher M. Burns, Stephen J. Hall, David J. Kelly, Stuart A Thompson

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33 Citations (Scopus)

Abstract

Campylobacter jejuni is a gastrointestinal pathogen of humans but can asymptomatically colonize the avian gut. C. jejuni therefore grows at both 37°C and 42°C, the internal temperatures of humans and birds respectively. Microarray and proteomic studies on temperature regulation in C. jejuni strain 81-176 revealed the upregulation at 42°C of two proteins, Cj0414 and Cj0415, orthologous to gluconate dehydrogenase (GADH) from Pectobacterium cypripedii. 81-176 demonstrated GADH activity, converting d-gluconate to 2-keto-d-gluconate, that was higher at 42°C than at 37°C. In contrast, cj0414 and cj0415 mutants lacked GADH activity. Wild-type but not cj0415 mutant bacteria exhibited gluconate-dependent respiration. Neither strain grew in defined media with d-gluconate or 2-keto-d-gluconate as a sole carbon source, revealing that gluconate was used as an electron donor rather than as a carbon source. When administered to chicks individually or in competition with wild-type, the cj0415 mutant was impaired in establishing colonization. In contrast, there were few significant differences in colonization of BALB/c-ByJ mice in single or mixed infections. These results suggest that the ability of C. jejuni to use gluconate as an electron donor via GADH activity is an important metabolic characteristic that is required for full colonization of avian but not mammalian hosts.

Original languageEnglish (US)
Pages (from-to)474-491
Number of pages18
JournalMolecular Microbiology
Volume68
Issue number2
DOIs
StatePublished - Apr 1 2008

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Campylobacter jejuni
Chickens
Oxidoreductases
Respiration
Temperature
Pectobacterium
gluconic acid
Carbon
Electrons
Coinfection
Proteomics
Birds
Up-Regulation
Bacteria

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

A temperature-regulated Campylobacter jejuni gluconate dehydrogenase is involved in respiration-dependent energy conservation and chicken colonization. / Pajaniappan, Mohanasundari; Hall, Johanna E.; Cawthraw, Shaun A.; Newell, Diane G.; Gaynor, Erin C.; Fields, Joshua A.; Rathbun, Kimberly M.; Agee, Willie A.; Burns, Christopher M.; Hall, Stephen J.; Kelly, David J.; Thompson, Stuart A.

In: Molecular Microbiology, Vol. 68, No. 2, 01.04.2008, p. 474-491.

Research output: Contribution to journalArticle

Pajaniappan, M, Hall, JE, Cawthraw, SA, Newell, DG, Gaynor, EC, Fields, JA, Rathbun, KM, Agee, WA, Burns, CM, Hall, SJ, Kelly, DJ & Thompson, SA 2008, 'A temperature-regulated Campylobacter jejuni gluconate dehydrogenase is involved in respiration-dependent energy conservation and chicken colonization', Molecular Microbiology, vol. 68, no. 2, pp. 474-491. https://doi.org/10.1111/j.1365-2958.2008.06161.x
Pajaniappan, Mohanasundari ; Hall, Johanna E. ; Cawthraw, Shaun A. ; Newell, Diane G. ; Gaynor, Erin C. ; Fields, Joshua A. ; Rathbun, Kimberly M. ; Agee, Willie A. ; Burns, Christopher M. ; Hall, Stephen J. ; Kelly, David J. ; Thompson, Stuart A. / A temperature-regulated Campylobacter jejuni gluconate dehydrogenase is involved in respiration-dependent energy conservation and chicken colonization. In: Molecular Microbiology. 2008 ; Vol. 68, No. 2. pp. 474-491.
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