Skip to main content
Top
Published in: Gut Pathogens 1/2010

Open Access 01-12-2010 | Hypothesis

Stress-induced survival strategies enable Salmonella Enteritidis to persistently colonize the chicken oviduct tissue and cope with antimicrobial factors in egg white: A hypothesis to explain a pandemic

Author: Filip Van Immerseel

Published in: Gut Pathogens | Issue 1/2010

Login to get access

Abstract

Background

Egg-associated transmission to humans seems to be characteristic of the Salmonella serotype Enteritidis, explaining why this particular serotype has caused a worldwide pandemic since the mid '80s. Salmonella Enteritidis is much more capable to persistently colonize the laying hen reproductive tract and to survive in the hostile egg white, as compared to other serotypes.

Presentation of the hypothesis

It is hypothesized that stress-induced survival mechanisms enable the serotype Enteritidis to persistently colonize the oviduct without causing damage and excessive inflammation, and to cope with the antimicrobial compounds present in egg white.

Testing the hypothesis

To test the hypothesis first of all Salmonella Enteritidis genes that are essential for colonization of the oviduct and survival in eggs need to be identified. Comparative genomics tools should be used to identify genes or pathogenicity islands that are present in Salmonella Enteritidis and not in the multiple non egg-contaminating serotypes. High-throughput signature-tagged-mutagenesis approaches, coupled to micro-array detection of the genes that lead to an attenuated phenotype when mutated is proposed as an ideal tool to identify genes involved in oviduct colonization and egg white survival. Identifying the stressors and antibacterial molecules in the oviduct and in the egg white that limit colonization or survival of non-Enteritidis serotypes is a second important objective that can theoretically be achieved using screenings of expressed oviduct cDNA libraries for their antibacterial activity against strains from multiple serotypes. Finally, the effect of contact with these stressors in the oviduct or egg white on Salmonella gene expression will need to be analyzed, in order to clarify whether serotype Enteritidis-specific regulation of certain stress-survival pathways are either or not present.

Implications of the hypothesis

Knowledge on the pathogenesis of egg infections would furthermore give insights that might be extrapolated to other biological interactions, in which a highly specialized bacterial pathogen resists the host response in a specific biological niche. In addition, this info can be of value in developing early warning criteria to identify emerging egg-associated Salmonella strains and in developing safe live attenuated vaccine strains.
Literature
1.
go back to reference Patrick ME, Adcock PM, Gomez TM, Altekruse SF, Holland BH, Tauxe RV: Salmonella Enteritidis infections, United States, 1985-1999. Emerg Infect Dis. 2004, 10: 1-7.PubMedCentralCrossRefPubMed Patrick ME, Adcock PM, Gomez TM, Altekruse SF, Holland BH, Tauxe RV: Salmonella Enteritidis infections, United States, 1985-1999. Emerg Infect Dis. 2004, 10: 1-7.PubMedCentralCrossRefPubMed
2.
go back to reference EFSA: The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. EFSA J. 223: 21-108. EFSA: The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. EFSA J. 223: 21-108.
3.
go back to reference Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R, Humphrey TJ, Van Immerseel F: Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Rev. 2009, 33: 718-738. 10.1111/j.1574-6976.2008.00161.x.CrossRefPubMed Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Gast R, Humphrey TJ, Van Immerseel F: Mechanisms of egg contamination by Salmonella Enteritidis. FEMS Microbiol Rev. 2009, 33: 718-738. 10.1111/j.1574-6976.2008.00161.x.CrossRefPubMed
4.
go back to reference Gast RK, Guraya R, Guard J, Holt PS: Multiplication of Salmonella Enteritidis in egg yolks after inoculation outside, on, and inside vitteline membranes and storage at different temperatures. J Food Prot. 2010, 73 (10): 1902-1906.PubMed Gast RK, Guraya R, Guard J, Holt PS: Multiplication of Salmonella Enteritidis in egg yolks after inoculation outside, on, and inside vitteline membranes and storage at different temperatures. J Food Prot. 2010, 73 (10): 1902-1906.PubMed
5.
go back to reference Gantois I, Eeckhaut V, Pasmans F, Haesebrouck F, Ducatelle R, Van Immerseel F: A comparative study on the pathogenesis of contamination by different serotypes of Salmonella. Avian Pathol. 2008, 37 (4): 399-406. 10.1080/03079450802216611.CrossRefPubMed Gantois I, Eeckhaut V, Pasmans F, Haesebrouck F, Ducatelle R, Van Immerseel F: A comparative study on the pathogenesis of contamination by different serotypes of Salmonella. Avian Pathol. 2008, 37 (4): 399-406. 10.1080/03079450802216611.CrossRefPubMed
6.
go back to reference Van Immerseel F, Raspoet R, Devloo R, De Vylder J, Gantois I, Pasmans F, Haesebrouck F, Ducatelle R: Which specific virulence traits enabled Salmonella serotype Enteritidis to cause a pandemic?. European Poultry Conference. Tours, France, 2010. Van Immerseel F, Raspoet R, Devloo R, De Vylder J, Gantois I, Pasmans F, Haesebrouck F, Ducatelle R: Which specific virulence traits enabled Salmonella serotype Enteritidis to cause a pandemic?. European Poultry Conference. Tours, France, 2010.
7.
go back to reference Mann K: The chicken egg white proteome. Proteomics. 2007, 7 (19): 3558-3568. 10.1002/pmic.200700397.CrossRefPubMed Mann K: The chicken egg white proteome. Proteomics. 2007, 7 (19): 3558-3568. 10.1002/pmic.200700397.CrossRefPubMed
8.
go back to reference Mann K: Proteomic analysis of the chicken egg vitelline membrane. Proteomics. 2008, 8 (11): 2322-2332. 10.1002/pmic.200800032.CrossRefPubMed Mann K: Proteomic analysis of the chicken egg vitelline membrane. Proteomics. 2008, 8 (11): 2322-2332. 10.1002/pmic.200800032.CrossRefPubMed
9.
go back to reference Réhault-Godbert S, Hervé-Grépinet V, Hincke M, Gautron J, Nys Y, Cabau C: Molecular defence of the chicken egg. Improving the safety and quality of eggs and egg products. Edited by: Nys Y, Bain M, Van Immerseel F. Woodhead Publishing, UK, Réhault-Godbert S, Hervé-Grépinet V, Hincke M, Gautron J, Nys Y, Cabau C: Molecular defence of the chicken egg. Improving the safety and quality of eggs and egg products. Edited by: Nys Y, Bain M, Van Immerseel F. Woodhead Publishing, UK,
10.
go back to reference Porwollik S, Santiviago CA, Cheng P, Florea L, Jackson S, McClelland M: Differences in gene content between Salmonella enterica serovar Enteritidis isolates and comparison to closely related serovars Gallinarum and Dublin. J Bacteriol. 2005, 187 (18): 6545-6555. 10.1128/JB.187.18.6545-6555.2005.PubMedCentralCrossRefPubMed Porwollik S, Santiviago CA, Cheng P, Florea L, Jackson S, McClelland M: Differences in gene content between Salmonella enterica serovar Enteritidis isolates and comparison to closely related serovars Gallinarum and Dublin. J Bacteriol. 2005, 187 (18): 6545-6555. 10.1128/JB.187.18.6545-6555.2005.PubMedCentralCrossRefPubMed
11.
go back to reference Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S, Churcher C, Qual MA, Stevens M, Jones MA, Watson M, Barron A, Layton A, Pickard D, Kingsley RA, Bignell A, Clark L, Harris B, Ormond D, Abdellah Z, Brooks K, Cherevach I, Chillingworth T, Woodward J, Norberczak H, Lord A, Arrowsmith C, Jagels K, Moule S, Mungall K, Sanders M, Whitehead S, Chabalgoity JA, Maskell D, Humphrey T, Roberts M, Barrow PA, Dougan G, Parkhill J: Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 2008, 18 (10): 1624-1637. 10.1101/gr.077404.108.PubMedCentralCrossRefPubMed Thomson NR, Clayton DJ, Windhorst D, Vernikos G, Davidson S, Churcher C, Qual MA, Stevens M, Jones MA, Watson M, Barron A, Layton A, Pickard D, Kingsley RA, Bignell A, Clark L, Harris B, Ormond D, Abdellah Z, Brooks K, Cherevach I, Chillingworth T, Woodward J, Norberczak H, Lord A, Arrowsmith C, Jagels K, Moule S, Mungall K, Sanders M, Whitehead S, Chabalgoity JA, Maskell D, Humphrey T, Roberts M, Barrow PA, Dougan G, Parkhill J: Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. Genome Res. 2008, 18 (10): 1624-1637. 10.1101/gr.077404.108.PubMedCentralCrossRefPubMed
12.
go back to reference Shivaprasad HL: Fowl typhoid and pullorum disease. Rev Sci Tech. 2000, 19: 405-424.PubMed Shivaprasad HL: Fowl typhoid and pullorum disease. Rev Sci Tech. 2000, 19: 405-424.PubMed
13.
go back to reference Chan K, Kim CC, Falkow S: Microarray-detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect Immun. 2005, 73 (9): 5438-5449. 10.1128/IAI.73.9.5438-5449.2005.PubMedCentralCrossRefPubMed Chan K, Kim CC, Falkow S: Microarray-detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect Immun. 2005, 73 (9): 5438-5449. 10.1128/IAI.73.9.5438-5449.2005.PubMedCentralCrossRefPubMed
14.
go back to reference Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, Monack DM: Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLOS Pathog. 2006, 2 (2): e11-10.1371/journal.ppat.0020011.PubMedCentralCrossRefPubMed Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, Monack DM: Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLOS Pathog. 2006, 2 (2): e11-10.1371/journal.ppat.0020011.PubMedCentralCrossRefPubMed
15.
go back to reference Keller LH, Benson CE, Krotec K, Eckroade RJ: Salmonella Enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect Immun. 1995, 63: 2443-2449.PubMedCentralPubMed Keller LH, Benson CE, Krotec K, Eckroade RJ: Salmonella Enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect Immun. 1995, 63: 2443-2449.PubMedCentralPubMed
16.
go back to reference Guard J, Gast RK, Guraya R: Colonization of avian reproductive tract tissues by variant subpopulations of Salmonella Enteritidis. Avian Dis. 2010, 54 (2): 857-861. 10.1637/9069-091109-Reg.1.CrossRefPubMed Guard J, Gast RK, Guraya R: Colonization of avian reproductive tract tissues by variant subpopulations of Salmonella Enteritidis. Avian Dis. 2010, 54 (2): 857-861. 10.1637/9069-091109-Reg.1.CrossRefPubMed
17.
go back to reference Gantois I, Pasmans F, Haesebrouck F, Ducatelle R, Van Immerseel F: Salmonella enterica serovar Enteritidis genes induced during oviduct colonization and egg contamination in laying hens. Appl Environ Microbiol. 2008, 74 (21): 6616-6622. 10.1128/AEM.01087-08.PubMedCentralCrossRefPubMed Gantois I, Pasmans F, Haesebrouck F, Ducatelle R, Van Immerseel F: Salmonella enterica serovar Enteritidis genes induced during oviduct colonization and egg contamination in laying hens. Appl Environ Microbiol. 2008, 74 (21): 6616-6622. 10.1128/AEM.01087-08.PubMedCentralCrossRefPubMed
18.
go back to reference Hincke MT, Gautron J, Tsang CP, McKee MD, Mys Y: Molecular cloning and ultrastructural localization of the core protein of an eggshell matrix proteoglycan, ovocleidin-116. J Biol Chem. 1999, 274 (46): 32915-32923. 10.1074/jbc.274.46.32915.CrossRefPubMed Hincke MT, Gautron J, Tsang CP, McKee MD, Mys Y: Molecular cloning and ultrastructural localization of the core protein of an eggshell matrix proteoglycan, ovocleidin-116. J Biol Chem. 1999, 274 (46): 32915-32923. 10.1074/jbc.274.46.32915.CrossRefPubMed
19.
go back to reference Gautron J, Murayama E, Vignal A, Morisson M, McKee MD, Rehault S, Labas V, Belghazi M, Vidal ML, Nys Y, Hincke MT: Cloning of ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins, bactericidal permeability-increasing proteins, and plunc family proteins. J Biol Chem. 2007, 282 (8): 5273-5286. 10.1074/jbc.M610294200.CrossRefPubMed Gautron J, Murayama E, Vignal A, Morisson M, McKee MD, Rehault S, Labas V, Belghazi M, Vidal ML, Nys Y, Hincke MT: Cloning of ovocalyxin-36, a novel chicken eggshell protein related to lipopolysaccharide-binding proteins, bactericidal permeability-increasing proteins, and plunc family proteins. J Biol Chem. 2007, 282 (8): 5273-5286. 10.1074/jbc.M610294200.CrossRefPubMed
20.
go back to reference Loit E, Wu K, Cheng X, Hincke MT, Altosaar I: Functional whole-colony screening method to identify antimicrobial proteins. J Microbiol Methods. 2008, 75 (3): 425-431. 10.1016/j.mimet.2008.07.023.CrossRefPubMed Loit E, Wu K, Cheng X, Hincke MT, Altosaar I: Functional whole-colony screening method to identify antimicrobial proteins. J Microbiol Methods. 2008, 75 (3): 425-431. 10.1016/j.mimet.2008.07.023.CrossRefPubMed
21.
go back to reference Raspoet R, De Smet L, Devloo R, Pasmans F, Haesebrouck F, Ducatelle R, Devreese B, Van Immerseel F: Multidrug efflux pumps confer resistance of Salmonella Enteritidis to egg white by the export of antimicrobial components through the tolC outer membrane channel. Proceedings of the Conference on the pathogenesis of bacterial diseases of animals. Prato, Italy, 2010. Raspoet R, De Smet L, Devloo R, Pasmans F, Haesebrouck F, Ducatelle R, Devreese B, Van Immerseel F: Multidrug efflux pumps confer resistance of Salmonella Enteritidis to egg white by the export of antimicrobial components through the tolC outer membrane channel. Proceedings of the Conference on the pathogenesis of bacterial diseases of animals. Prato, Italy, 2010.
Metadata
Title
Stress-induced survival strategies enable Salmonella Enteritidis to persistently colonize the chicken oviduct tissue and cope with antimicrobial factors in egg white: A hypothesis to explain a pandemic
Author
Filip Van Immerseel
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2010
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/1757-4749-2-23

Other articles of this Issue 1/2010

Gut Pathogens 1/2010 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.