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Increased intracellular calcium level and impaired nutrient absorption are important pathogenicity traits in the chicken intestinal epithelium during Campylobacter jejuni colonization

  • Applied microbial and cell physiology
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Abstract

Although a high number of chickens carry Campylobacter jejuni, the mechanistic action of colonization in the intestine is still poorly understood. The current study was therefore designed to investigate the effects of C. jejuni on glucose uptake, amino acids availability in digesta, and intracellular calcium [Ca2+]i signaling in the intestines of broiler chickens. For this, we compared: control birds (n = 60) and C. jejuni-infected birds (n = 60; infected orally with 1 × 108 CFU of C. jejuni NCTC 12744 at 14 days of age). Our results showed that glucose uptake was reduced due to C. jejuni infection in isolated jejunal, but not in cecal mucosa at 14 days postinfection (dpi). The decrease in intestinal glucose absorption coincided with a decrease in body weight gain during the 2-week post-infectious period. A reduction in the amount of the amino acids (serine, proline, valine, leucine, phenylalanine, arginine, histidine, and lysine) in ileal digesta of the infected birds at 2 and/or 7 dpi was found, indicating that Campylobacter utilizes amino acids as a carbon source for their multiplication. Applying the cell-permeable Ca2+ indicator Fluo-4 and two-photon microscopy, we revealed that [Ca2+]i was increased in the jejunal and cecal mucosa of infected birds. The muscarinic agonist carbachol induced an increase in [Ca2+]i in jejunum and cecum mucosa of control chickens, a response absent in the mucosa of infected chickens, demonstrating that the modulation of [Ca2+]i by Campylobacter might be involved in facilitating the necessary cytoskeletal rearrangements that occur during the bacterial invasion of epithelial cells. In conclusion, this study demonstrates the multifaceted interactions of C. jejuni with the gastrointestinal mucosa of broiler chickens. For the first time, it could be shown that a Campylobacter infection could interfere with intracellular Ca2+ signaling and nutrient absorption in the small intestine with consequences on intestinal function, performance, and Campylobacter colonization. Altogether, these findings indicate that Campylobacter is not entirely a commensal and can be recognized as an important factor contributing to an impaired chicken gut health.

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Acknowledgments

This work was financed within the Center of Excellence for Poultry (CEPO) project, which is funded by the European Regional Development Fund, Cross-border Cooperation Programme Austria–Hungary 2007–2013. Grant No: L00112. Furthermore, the authors gratefully thank the Alexander von Humboldt Foundation, Bonn, Germany, for supporting Wageha Awad as a visiting Fellowship for experienced researchers to the Free University of Berlin, Germany. Finally, we would like to thank all staff who assisted with the animal infection experiments at the Clinic for Poultry and Fish Medicine, Vienna.

Ethics statement

The animal experiment was approved by the institutional ethics committee of the University of Veterinary Medicine and the Ministry of Research and Science under license number GZ 68.205/0011-11/3b/2013. This study was performed in strict accordance to the European Union and Austria’s regulations for the use and care of animals. All husbandry practices were performed with full consideration of animal welfare.

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Authors and Affiliations

  1. Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine, Vienna, Austria

    Wageha A. Awad, Claudia Hess, Basel Khayal & Michael Hess

  2. Institute of Veterinary Physiology, Department of Veterinary Medicine, Free University of Berlin, Berlin, Germany

    Alina Smorodchenko & Jörg R. Aschenbach

  3. Department of Animal Science and Animal Husbandry, Georgikon Faculty, University of Pannonia, Keszthely, Hungary

    Andor Molnár & Károly Dublecz

  4. Institute of Physiology, Pathophysiology and Biophysics, Department of Biomedical Sciences, University of Veterinary Medicine, Vienna, Austria

    Alina Smorodchenko & Elena E. Pohl

  5. Department of Animal Hygiene, Poultry and Environment, Faculty of Veterinary Medicine, South Valley University, Qena, Egypt

    Wageha A. Awad

  6. Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine, Vienna, Austria

    Andor Molnár

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  1. Wageha A. Awad
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  2. Alina Smorodchenko
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  3. Claudia Hess
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  4. Jörg R. Aschenbach
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  6. Károly Dublecz
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  7. Basel Khayal
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  8. Elena E. Pohl
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  9. Michael Hess
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Correspondence to Wageha A. Awad.

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Awad, W.A., Smorodchenko, A., Hess, C. et al. Increased intracellular calcium level and impaired nutrient absorption are important pathogenicity traits in the chicken intestinal epithelium during Campylobacter jejuni colonization. Appl Microbiol Biotechnol 99, 6431–6441 (2015). https://doi.org/10.1007/s00253-015-6543-z

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  • DOI: https://doi.org/10.1007/s00253-015-6543-z

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