Tags

Type your tag names separated by a space and hit enter

Salmonella enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses To Overcome Colonization Resistance in Swine.
Appl Environ Microbiol. 2020 10 15; 86(21)AE

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.

Authors+Show Affiliations

Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada. Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada.Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada. Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada.Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada.Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada Richard.Uwiera@ualberta.ca Douglas.Inglis@canada.ca.Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, Alberta, Canada Richard.Uwiera@ualberta.ca Douglas.Inglis@canada.ca.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

32859592

Citation

Bescucci, Danisa M., et al. "Salmonella Enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses to Overcome Colonization Resistance in Swine." Applied and Environmental Microbiology, vol. 86, no. 21, 2020.
Bescucci DM, Moote PE, Ortega Polo R, et al. Salmonella enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses To Overcome Colonization Resistance in Swine. Appl Environ Microbiol. 2020;86(21).
Bescucci, D. M., Moote, P. E., Ortega Polo, R., Uwiera, R. R. E., & Inglis, G. D. (2020). Salmonella enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses To Overcome Colonization Resistance in Swine. Applied and Environmental Microbiology, 86(21). https://doi.org/10.1128/AEM.01569-20
Bescucci DM, et al. Salmonella Enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses to Overcome Colonization Resistance in Swine. Appl Environ Microbiol. 2020 10 15;86(21) PubMed PMID: 32859592.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Salmonella enterica Serovar Typhimurium Temporally Modulates the Enteric Microbiota and Host Responses To Overcome Colonization Resistance in Swine. AU - Bescucci,Danisa M, AU - Moote,Paul E, AU - Ortega Polo,Rodrigo, AU - Uwiera,Richard R E, AU - Inglis,G Douglas, Y1 - 2020/10/15/ PY - 2020/06/30/received PY - 2020/08/19/accepted PY - 2020/8/30/pubmed PY - 2020/12/2/medline PY - 2020/8/30/entrez KW - Salmonella enterica serovar Typhimurium KW - colonization resistance KW - salmonellosis KW - swine KW - temporal host and microbiota responses JF - Applied and environmental microbiology JO - Appl Environ Microbiol VL - 86 IS - 21 N2 - 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. SN - 1098-5336 UR - https://www.unboundmedicine.com/medline/citation/32859592/Salmonella_enterica_Serovar_Typhimurium_Temporally_Modulates_the_Enteric_Microbiota_and_Host_Responses_To_Overcome_Colonization_Resistance_in_Swine_ L2 - https://journals.asm.org/doi/10.1128/AEM.01569-20?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -