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Microbial Ecology

Salmonella enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses To Overcome Colonization Resistance in Swine

Danisa M. Bescucci, Paul E. Moote, Rodrigo Ortega Polo, Richard R. E. Uwiera, G. Douglas Inglis
Christopher A. Elkins, Editor
Danisa M. Bescucci
aLethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
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Paul E. Moote
aLethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
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Rodrigo Ortega Polo
aLethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada
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  • ORCID record for Rodrigo Ortega Polo
Richard R. E. Uwiera
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
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G. Douglas Inglis
aLethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada
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Christopher A. Elkins
Centers for Disease Control and Prevention
Roles: Editor
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DOI: 10.1128/AEM.01569-20
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ABSTRACT

Salmonella enterica serovar Typhimurium is a prevalent incitant of enteritis in human beings and nonhuman animals. It has been proposed that host defense responses incited by Salmonella allow the bacterium to overcome colonization resistance. Piglets (n = 24) were orally inoculated with S. enterica serovar Typhimurium DT104 or buffer alone, and the host and microbial responses were temporally examined at the acute (2 days postinoculation [dpi]), subacute (6 dpi), and recovery (10 dpi) stages of salmonellosis. At the acute stage of disease, body temperatures were elevated, and feed consumption and weight gain were reduced. The densities of Salmonella associated with the gut mucosa decreased over time, with higher densities of the bacterium in the ileum and the large intestine. Moreover, substantive histopathological changes were observed as a function of time, with prominent epithelial injury and neutrophil infiltration observed at 2 dpi. Correspondingly, a variety of host metrics were temporally affected in piglets with salmonellosis (e.g., TNFα, IFNγ, PR39, βD2, iNOS, IL8, REGIIIγ). The enteric microbiota was characterized using culture-independent and -dependent methods in concert, and taxon- and location-specific changes to the microbiota were observed in infected piglets. Bacteroides spp. (e.g., Bacteroides uniformis, Bacteroides fragilis), Streptococcus spp. (e.g., Streptococcus gallolyticus), and various Gammaproteobacteria were highly associated with inflamed tissues, while bacteria within the Ruminococcaceae and Veillonellaceae families were mainly associated with healthy mucosae. In conclusion, the study findings showed that S. Typhimurium incited temporal and spatial modifications to the swine autochthonous microbiota, and to host defense responses, that were consistent with overcoming colonization resistance to incite salmonellosis in swine.

IMPORTANCE Limited information is available on host and enteric microbiota responses incited by Salmonella enterica serovar Typhimurium in swine and on possible mechanisms by which the bacterium overcomes colonization resistance to incite salmonellosis. Temporal characterization of a variety of host metrics in piglets (e.g., physiological, histopathological, and immunological) showed the importance of studying the progression of salmonellosis. A number of host responses integrally associated with disease development were identified. Utilization of next-generation sequence analysis to characterize the enteric microbiota was found to lack sufficient resolution; however, culture-dependent and -independent methods in combination identified taxon- and location-specific changes to bacterial communities in infected piglets. The study identified bacterial and host responses associated with salmonellosis, which will be beneficial in understanding colonization resistance and in the development of effective alternatives to antibiotics to mitigate salmonellosis.

FOOTNOTES

    • Received 30 June 2020.
    • Accepted 19 August 2020.
    • Accepted manuscript posted online 28 August 2020.
  • Supplemental material is available online only.

  • © Crown copyright 2020.

The government of Australia, Canada, or the UK (“the Crown”) owns the copyright interests of authors who are government employees. The Crown Copyright is not transferable.

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Salmonella enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses To Overcome Colonization Resistance in Swine
Danisa M. Bescucci, Paul E. Moote, Rodrigo Ortega Polo, Richard R. E. Uwiera, G. Douglas Inglis
Applied and Environmental Microbiology Oct 2020, 86 (21) e01569-20; DOI: 10.1128/AEM.01569-20

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Salmonella enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses To Overcome Colonization Resistance in Swine
Danisa M. Bescucci, Paul E. Moote, Rodrigo Ortega Polo, Richard R. E. Uwiera, G. Douglas Inglis
Applied and Environmental Microbiology Oct 2020, 86 (21) e01569-20; DOI: 10.1128/AEM.01569-20
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KEYWORDS

Salmonella enterica serovar Typhimurium
swine
colonization resistance
salmonellosis
temporal host and microbiota responses

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