Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs

ABSTRACT Salmonella colonization and infection in production animals such as pigs are a cause for concern from a public health perspective. Variations in susceptibility to natural infection may be influenced by the intestinal microbiota. Using 16S rRNA compositional sequencing, we characterized the...

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Autores principales:	Héctor Argüello, Jordi Estellé, Finola C. Leonard, Fiona Crispie, Paul D. Cotter, Orla O’Sullivan, Helen Lynch, Kavita Walia, Geraldine Duffy, Peadar G. Lawlor, Gillian E. Gardiner
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	microbiome colonization resistance metagenome pathogen pig Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f6f7ac484d3f490abe7382245ea53fb8
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spelling	oai:doaj.org-article:f6f7ac484d3f490abe7382245ea53fb82021-12-02T18:39:15ZInfluence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs10.1128/mSystems.00021-192379-5077https://doaj.org/article/f6f7ac484d3f490abe7382245ea53fb82019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00021-19https://doaj.org/toc/2379-5077ABSTRACT Salmonella colonization and infection in production animals such as pigs are a cause for concern from a public health perspective. Variations in susceptibility to natural infection may be influenced by the intestinal microbiota. Using 16S rRNA compositional sequencing, we characterized the fecal microbiome of 15 weaned pigs naturally infected with Salmonella at 18, 33, and 45 days postweaning. Dissimilarities in microbiota composition were analyzed in relation to Salmonella infection status (infected, not infected), serological status, and shedding pattern (nonshedders, single-point shedders, intermittent-persistent shedders). Global microbiota composition was associated with the infection outcome based on serological analysis. Greater richness within the microbiota postweaning was linked to pigs being seronegative at the end of the study at 11 weeks of age. Members of the Clostridia, such as Blautia, Roseburia, and Anaerovibrio, were more abundant and part of the core microbiome in nonshedder pigs. Cellulolytic microbiota (Ruminococcus and Prevotella) were also more abundant in noninfected pigs during the weaning and growing stages. Microbial profiling also revealed that infected pigs had a higher abundance of Lactobacillus and Oscillospira, the latter also being part of the core microbiome of intermittent-persistent shedders. These findings suggest that a lack of microbiome maturation and greater proportions of microorganisms associated with suckling increase susceptibility to infection. In addition, the persistence of Salmonella shedding may be associated with an enrichment of pathobionts such as Anaerobiospirillum. Overall, these results suggest that there may be merit in manipulating certain taxa within the porcine intestinal microbial community to increase disease resistance against Salmonella in pigs. IMPORTANCE Salmonella is a global threat for public health, and pork is one of the main sources of human salmonellosis. However, the complex epidemiology of the infection limits current control strategies aimed at reducing the prevalence of this infection in pigs. The present study analyzes for the first time the impact of the gut microbiota in Salmonella infection in pigs and its shedding pattern in naturally infected growing pigs. Microbiome (16S rRNA amplicon) analysis reveals that maturation of the gut microbiome could be a key consideration with respect to limiting the infection and shedding of Salmonella in pigs. Indeed, seronegative animals had higher richness of the gut microbiota early after weaning, and uninfected pigs had higher abundance of strict anaerobes from the class Clostridia, results which demonstrate that a fast transition from the suckling microbiota to a postweaning microbiota could be crucial with respect to protecting the animals.Héctor ArgüelloJordi EstelléFinola C. LeonardFiona CrispiePaul D. CotterOrla O’SullivanHelen LynchKavita WaliaGeraldine DuffyPeadar G. LawlorGillian E. GardinerAmerican Society for Microbiologyarticlemicrobiomecolonization resistancemetagenomepathogenpigMicrobiologyQR1-502ENmSystems, Vol 4, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	microbiome colonization resistance metagenome pathogen pig Microbiology QR1-502
spellingShingle	microbiome colonization resistance metagenome pathogen pig Microbiology QR1-502 Héctor Argüello Jordi Estellé Finola C. Leonard Fiona Crispie Paul D. Cotter Orla O’Sullivan Helen Lynch Kavita Walia Geraldine Duffy Peadar G. Lawlor Gillian E. Gardiner Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs
description	ABSTRACT Salmonella colonization and infection in production animals such as pigs are a cause for concern from a public health perspective. Variations in susceptibility to natural infection may be influenced by the intestinal microbiota. Using 16S rRNA compositional sequencing, we characterized the fecal microbiome of 15 weaned pigs naturally infected with Salmonella at 18, 33, and 45 days postweaning. Dissimilarities in microbiota composition were analyzed in relation to Salmonella infection status (infected, not infected), serological status, and shedding pattern (nonshedders, single-point shedders, intermittent-persistent shedders). Global microbiota composition was associated with the infection outcome based on serological analysis. Greater richness within the microbiota postweaning was linked to pigs being seronegative at the end of the study at 11 weeks of age. Members of the Clostridia, such as Blautia, Roseburia, and Anaerovibrio, were more abundant and part of the core microbiome in nonshedder pigs. Cellulolytic microbiota (Ruminococcus and Prevotella) were also more abundant in noninfected pigs during the weaning and growing stages. Microbial profiling also revealed that infected pigs had a higher abundance of Lactobacillus and Oscillospira, the latter also being part of the core microbiome of intermittent-persistent shedders. These findings suggest that a lack of microbiome maturation and greater proportions of microorganisms associated with suckling increase susceptibility to infection. In addition, the persistence of Salmonella shedding may be associated with an enrichment of pathobionts such as Anaerobiospirillum. Overall, these results suggest that there may be merit in manipulating certain taxa within the porcine intestinal microbial community to increase disease resistance against Salmonella in pigs. IMPORTANCE Salmonella is a global threat for public health, and pork is one of the main sources of human salmonellosis. However, the complex epidemiology of the infection limits current control strategies aimed at reducing the prevalence of this infection in pigs. The present study analyzes for the first time the impact of the gut microbiota in Salmonella infection in pigs and its shedding pattern in naturally infected growing pigs. Microbiome (16S rRNA amplicon) analysis reveals that maturation of the gut microbiome could be a key consideration with respect to limiting the infection and shedding of Salmonella in pigs. Indeed, seronegative animals had higher richness of the gut microbiota early after weaning, and uninfected pigs had higher abundance of strict anaerobes from the class Clostridia, results which demonstrate that a fast transition from the suckling microbiota to a postweaning microbiota could be crucial with respect to protecting the animals.
format	article
author	Héctor Argüello Jordi Estellé Finola C. Leonard Fiona Crispie Paul D. Cotter Orla O’Sullivan Helen Lynch Kavita Walia Geraldine Duffy Peadar G. Lawlor Gillian E. Gardiner
author_facet	Héctor Argüello Jordi Estellé Finola C. Leonard Fiona Crispie Paul D. Cotter Orla O’Sullivan Helen Lynch Kavita Walia Geraldine Duffy Peadar G. Lawlor Gillian E. Gardiner
author_sort	Héctor Argüello
title	Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs
title_short	Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs
title_full	Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs
title_fullStr	Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs
title_full_unstemmed	Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs
title_sort	influence of the intestinal microbiota on colonization resistance to <italic toggle="yes">salmonella</italic> and the shedding pattern of naturally exposed pigs
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/f6f7ac484d3f490abe7382245ea53fb8
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Influence of the Intestinal Microbiota on Colonization Resistance to <italic toggle="yes">Salmonella</italic> and the Shedding Pattern of Naturally Exposed Pigs

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