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Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis

BACKGROUND: Clinical intervention during bacterial infections in farm animals such as pigs commonly includes the use of antimicrobials. With the rise of antimicrobial resistance and the attempts to reduce the use of antibiotics in food animals, effective alternatives are urgently needed to reduce or...

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Autores principales: Muwonge, Adrian, Karuppannan, Anbu K., Opriessnig, Tanja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7931366/
https://www.ncbi.nlm.nih.gov/pubmed/33663618
http://dx.doi.org/10.1186/s42523-021-00084-6
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author Muwonge, Adrian
Karuppannan, Anbu K.
Opriessnig, Tanja
author_facet Muwonge, Adrian
Karuppannan, Anbu K.
Opriessnig, Tanja
author_sort Muwonge, Adrian
collection PubMed
description BACKGROUND: Clinical intervention during bacterial infections in farm animals such as pigs commonly includes the use of antimicrobials. With the rise of antimicrobial resistance and the attempts to reduce the use of antibiotics in food animals, effective alternatives are urgently needed to reduce or even remove pathogens and disease risks. Improving clinical outcomes and overall pig health by using probiotics appears attractive. However, reliable data sets on the efficacy of probiotics are scarce. The obligate intracellular bacterium Lawsonia intracellularis is widespread in pigs and associated with severe enteropathy, mainly in the ileum, commonly resulting in substantial reduction in weight gain. The impact of three in-feed probiotics and a commercial live L. intracellularis vaccine was compared in a pig challenge model. Probiotic treatment was associated with reduced L. intracellularis fecal shedding and reduced gut lesions. Here, the bacterial microbiota of the ileum of these pigs was characterized with 16S rRNA gene sequencing and was subsequently analyzed with bioinformatics tools. RESULTS: The greatest microbial richness was observed in the probiotic treated group T03-LAW, which accounted for 87% of richness observed in the study. Treatment had a significant impact on both the microbiota structure and taxonomic profile in the ileum, explaining between 26 and 36% of the structural variation, with the strongest association in the T03-LAW group. Overall, the largest changes were observed for the pigs treated with in-feed Bacillus pumilus; the microbiota of these pigs had the greatest diversity and highest richness. We also observed depleted and enriched core microbiota amongst the groups; however, there was no correlation with clinical characteristics. The results suggest that an increased diversity of the ileal microbiota is associated with a reduction in shedding, i.e. a unit increase in Shannon diversity index resulted in 2.8 log reduction in shedding. CONCLUSIONS: Probiotic supplementation of a base feed ration increased ileum microbiota diversity leading to a mitigation of the effects of a pathogenic L. intracellularis challenge. An even and diverse microbiota community benefits pigs infected with L. intracellularis, however, investigations are needed to determine if this is also true for other pathogens. The study unambiguously demonstrates the usefulness of probiotic supplementation in reducing the impact of enteric pathogens and pathogen shedding rates in food animals without the use of antimicrobials. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00084-6.
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spelling pubmed-79313662021-03-08 Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis Muwonge, Adrian Karuppannan, Anbu K. Opriessnig, Tanja Anim Microbiome Research Article BACKGROUND: Clinical intervention during bacterial infections in farm animals such as pigs commonly includes the use of antimicrobials. With the rise of antimicrobial resistance and the attempts to reduce the use of antibiotics in food animals, effective alternatives are urgently needed to reduce or even remove pathogens and disease risks. Improving clinical outcomes and overall pig health by using probiotics appears attractive. However, reliable data sets on the efficacy of probiotics are scarce. The obligate intracellular bacterium Lawsonia intracellularis is widespread in pigs and associated with severe enteropathy, mainly in the ileum, commonly resulting in substantial reduction in weight gain. The impact of three in-feed probiotics and a commercial live L. intracellularis vaccine was compared in a pig challenge model. Probiotic treatment was associated with reduced L. intracellularis fecal shedding and reduced gut lesions. Here, the bacterial microbiota of the ileum of these pigs was characterized with 16S rRNA gene sequencing and was subsequently analyzed with bioinformatics tools. RESULTS: The greatest microbial richness was observed in the probiotic treated group T03-LAW, which accounted for 87% of richness observed in the study. Treatment had a significant impact on both the microbiota structure and taxonomic profile in the ileum, explaining between 26 and 36% of the structural variation, with the strongest association in the T03-LAW group. Overall, the largest changes were observed for the pigs treated with in-feed Bacillus pumilus; the microbiota of these pigs had the greatest diversity and highest richness. We also observed depleted and enriched core microbiota amongst the groups; however, there was no correlation with clinical characteristics. The results suggest that an increased diversity of the ileal microbiota is associated with a reduction in shedding, i.e. a unit increase in Shannon diversity index resulted in 2.8 log reduction in shedding. CONCLUSIONS: Probiotic supplementation of a base feed ration increased ileum microbiota diversity leading to a mitigation of the effects of a pathogenic L. intracellularis challenge. An even and diverse microbiota community benefits pigs infected with L. intracellularis, however, investigations are needed to determine if this is also true for other pathogens. The study unambiguously demonstrates the usefulness of probiotic supplementation in reducing the impact of enteric pathogens and pathogen shedding rates in food animals without the use of antimicrobials. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-021-00084-6. BioMed Central 2021-03-04 /pmc/articles/PMC7931366/ /pubmed/33663618 http://dx.doi.org/10.1186/s42523-021-00084-6 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research Article
Muwonge, Adrian
Karuppannan, Anbu K.
Opriessnig, Tanja
Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis
title Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis
title_full Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis
title_fullStr Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis
title_full_unstemmed Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis
title_short Probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of Lawsonia intracellularis
title_sort probiotics mediated gut microbiota diversity shifts are associated with reduction in histopathology and shedding of lawsonia intracellularis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7931366/
https://www.ncbi.nlm.nih.gov/pubmed/33663618
http://dx.doi.org/10.1186/s42523-021-00084-6
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