Evaluation of the control of pathogen load by an anti-Salmonella bacterium in a herd of cattle with persistent Salmonella infection

Toni G. Patton Pre-Harvest Food Safety and Enteric Diseases Research Unit, National Animal Disease Center, USDA, Agricultural Research Service, 2300 Dayton Rd, Ames, IA 50010

Search for other papers by Toni G. Patton in
Current site
Google Scholar
PubMed
Close
 PhD
,
Vijay K. Sharma Pre-Harvest Food Safety and Enteric Diseases Research Unit, National Animal Disease Center, USDA, Agricultural Research Service, 2300 Dayton Rd, Ames, IA 50010

Search for other papers by Vijay K. Sharma in
Current site
Google Scholar
PubMed
Close
 PhD
, and
Steve A. Carlson Department of Biomedical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA 50011

Search for other papers by Steve A. Carlson in
Current site
Google Scholar
PubMed
Close
 DVM, PhD

Abstract

Objective—To determine whether an anti-Salmonella bacterium is involved in control of pathogen load in persistently infected cattle herds.

Animals—24 Holstein calves experimentally infected and 39 Holstein cows naturally infected with Salmonella spp.

Procedures—An Escherichia coli (designated as P8E5) that possessed anti-Salmonella activity was isolated from Salmonella-negative bovine feces obtained from a herd with endemic Salmonella infection. In vitro analysis involved enumerating Salmonella enterica serovar Typhimurium coincubated with E coli P8E5. In vivo analysis involved coadministration of Salmonella spp and E coli P8E5 or an E coli control strain to neonatal Holstein calves. Fecal samples were collected on multiple days after inoculation, and quantitative PCR assay was performed by use of Salmonella-specific primers.

ResultsE coli P8E5 reduced viability of Salmonella spp in vitro. Shedding of Salmonella organisms was diminished in calves administered E coli P8E5, whereas the control strain of E coli had no effect on shedding of Salmonella organisms.

Conclusions and Clinical Relevance—In this study, an E coli strain was identified that possessed bacteriocin-like activity and was able to decrease viability of Salmonella organisms in vitro and in vivo. Therefore, it is possible that this organism could be representative of native microbiota that dampen Salmonella spp in persistently infected cattle herds.

Abstract

Objective—To determine whether an anti-Salmonella bacterium is involved in control of pathogen load in persistently infected cattle herds.

Animals—24 Holstein calves experimentally infected and 39 Holstein cows naturally infected with Salmonella spp.

Procedures—An Escherichia coli (designated as P8E5) that possessed anti-Salmonella activity was isolated from Salmonella-negative bovine feces obtained from a herd with endemic Salmonella infection. In vitro analysis involved enumerating Salmonella enterica serovar Typhimurium coincubated with E coli P8E5. In vivo analysis involved coadministration of Salmonella spp and E coli P8E5 or an E coli control strain to neonatal Holstein calves. Fecal samples were collected on multiple days after inoculation, and quantitative PCR assay was performed by use of Salmonella-specific primers.

ResultsE coli P8E5 reduced viability of Salmonella spp in vitro. Shedding of Salmonella organisms was diminished in calves administered E coli P8E5, whereas the control strain of E coli had no effect on shedding of Salmonella organisms.

Conclusions and Clinical Relevance—In this study, an E coli strain was identified that possessed bacteriocin-like activity and was able to decrease viability of Salmonella organisms in vitro and in vivo. Therefore, it is possible that this organism could be representative of native microbiota that dampen Salmonella spp in persistently infected cattle herds.

  • 1.

    Baird-Parker AC. Foodborne salmonellosis. Lancet 1990;336:12311235.

  • 2.

    Davis MA, Hancock DD, Besser TE. Multiresistant clones of Salmonella enterica: the importance of dissemination. J Lab Clin Med 2002;140:135141.

  • 3.

    Humphrey T. Salmonella, stress responses and food safety. Nat Rev Microbiol 2004;2:504509.

  • 4.

    Becker PM. Physiological Achilles' heels of enteropathogenic bacteria in livestock. Curr Issues Intest Microbiol 2005;6:3154.

  • 5.

    Fuller R. Probiotics in man and animals. J Appl Bacteriol 1989;66:365378.

  • 6.

    Nava GM, Bielke LR, Callaway TR, et al. Probiotic alternatives to reduce gastrointestinal infections: the poultry experience. Anim Health Res Rev 2005;6:105118.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Gillor O, Kirkup BC, Riley MA. Colicins and microcins: the next generation antimicrobials. Adv Appl Microbiol 2004;54:129146.

  • 8.

    Danyluk MD, Zhao T, Doyle MP. Competitive inhibition bacteria of bovine origin against Salmonella serovars. J Food Prot 2007;70:18041810.

  • 9.

    Vollaard EJ, Clasener HA. Colonization resistance. Antimicrob Agents Chemother 1994;38:409414.

  • 10.

    Lorenzo V, Aguilar A. Antibiotics from gram-negative bacteria: do they play a role in microbial ecology? Trends Biochem Sci 1984;9:266269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Stern NJ, Svetoch EA, Eruslanov BV, et al. Isolation of a Lactobacillus salivarius strain and purification of its bacteriocin, which is inhibitory to Campylobacter jejuni in the chicken gastrointestinal system. Antimicrob Agents Chemother 2006;50:31113116.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Baquero F, Moreno F. The microcins. FEMS Microbiol Lett 1984;23:117124.

  • 13.

    Daw MA, Falkiner FR. Bacteriocins: nature, function and structure. Micron 1996;27:467479.

  • 14.

    Zhao T, Doyle MP, Harmon BG, et al. Reduction of carriage of enterohemorrhagic Escherichia coli O157:H7 in cattle by inoculation with probiotic bacteria. J Clin Microbiol 1998;36:641647.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Stern NJ, Svetoch EA, Eruslanov BV, et al. Paenibacillus polymyxa purified bacteriocin to control Campylobacter jejuni in chickens. J Food Prot 2005;68:14501453.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Etcheverria AI, Arroyo GH, Perdigon G, et al. Escherichia coli with anti-O157:H7 activity isolated from bovine colon. J Appl Microbiol 2006;100:384389.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Gough JM, Conlan LL, Denman SE, et al. Screening of bacteria from the cattle gastrointestinal tract for inhibitory activity against enterohemorrhagic Escherichia coli O157:H7, O111:H-, and O26:H11. J Food Prot 2006;69:28432850.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Leverentz B, Conway WS, Janisiewicz W, et al. Biocontrol of the food-borne pathogens Listeria monocytogenes and Salmonella enterica serovar Poona on fresh-cut apples with naturally occurring bacterial and yeast antagonists. Appl Environ Microbiol 2006;72:11351140.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Simonova M, Laukova A. Bacteriocin activity of enterococci from rabbits. Vet Res Commun 2007;31:143152.

  • 20.

    Carlson SA, Willson RM, Crane AJ, et al. Evaluation of invasionconferring genotypes and antibiotic-induced hyperinvasive phenotypes in multiple antibiotic resistant Salmonella typhimurium DT104. Microb Pathog 2000;28:373378.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Penheiter KL, Mathur N, Giles D, et al. Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer's patches. Mol Microbiol 1997;24:697709.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Boyd EF, Wang FS, Beltran P, et al. Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I. J Gen Microbiol 1993;139:11251132.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Carlson SA, Bolton LF, Briggs CE, et al. Detection of multiresistant Salmonella typhimurium DT104 using multiplex and fluorogenic PCR. Mol Cell Probes 1999;13:213222.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Sharma VK, Carlson SA. Simultaneous detection of Salmonella strains and Escherichia coli O157:H7 with fluorogenic PCR and single-enrichment-broth culture. Appl Environ Microbiol 2000;66:54725476.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Carlson SA, Sharma VK, McCuddin ZP, et al. Involvement of a Salmonella genomic island 1 gene in the rumen protozoanmediated enhancement of invasion for multiple-antibiotic-resistant Salmonella enterica serovar Typhimurium. Infect Immun 2007;75:792800.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Helgerson AF, Sharma V, Dow AM, et al. Edema disease caused by a clone of Escherichia coli O147. J Clin Microbiol 2006;44:30743077.

  • 27.

    Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk and dilution susceptibility tests. Wayne, Pa: Clinical and Laboratory Standards Institute, 2001;1718.

    • Search Google Scholar
    • Export Citation
  • 28.

    Riley MA, Gordon DM. The ecological role of bacteriocins in bacterial competition. Trends Microbiol 1999;7:129133.

  • 29.

    James R, Kleanthous C, Moore GR. The biology of E colicins: paradigms and paradoxes. Microbiology 1996;142:15691580.

  • 30.

    Gordon DM, O'Brien CL. Bacteriocin diversity and the frequency of multiple bacteriocin production in Escherichia coli. Microbiology 2006;152:32393244.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Destoumieux-Garzon D, Peduzzi J, Rebuffat S. Focus on modified microcins: structural features and mechanisms of action. Biochimie 2002;84:511519.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Kerr B, Riley MA, Feldman MW, et al. Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 2002;418:171174.

  • 33.

    Kirkup BC, Riley MA. Antibiotic-mediated antagonism leads to a bacterial game of rock-paper-scissors in vivo. Nature 2004;428:412414.

Advertisement