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Essential role of invasin for colonization and persistence of Yersinia enterocolitica in its natural reservoir host, the pig.

ABSTRACT: In this study, an oral minipig infection model was established to investigate the pathogenicity of Yersinia enterocolitica bioserotype 4/O:3. O:3 strains are highly prevalent in pigs, which are usually symptomless carriers, and they represent the most common cause of human yersiniosis. To assess the pathogenic potential of the O:3 serotype, we compared the colonization properties of Y. enterocolitica O:3 with O:8, a highly mouse-virulent Y. enterocolitica serotype, in minipigs and mice. We found that O:3 is a significantly better colonizer of swine than is O:8. Coinfection studies with O:3 mutant strains demonstrated that small variations within the O:3 genome leading to higher amounts of the primary adhesion factor invasin (InvA) improved colonization and/or survival of this serotype in swine but had only a minor effect on the colonization of mice. We further demonstrated that a deletion of the invA gene abolished long-term colonization in the pigs. Our results indicate a primary role for invasin in naturally occurring Y. enterocolitica O:3 infections in pigs and reveal a higher adaptation of O:3 than O:8 strains to their natural pig reservoir host.

SUBMITTER: Schaake J

PROVIDER: S-EPMC3958021 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

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Essential role of invasin for colonization and persistence of Yersinia enterocolitica in its natural reservoir host, the pig.

Schaake Julia J Drees Anna A Grüning Petra P Uliczka Frank F Pisano Fabio F Thiermann Tanja T von Altrock Alexandra A Seehusen Frauke F Valentin-Weigand Peter P Dersch Petra P

Infection and immunity 20131216 3

In this study, an oral minipig infection model was established to investigate the pathogenicity of Yersinia enterocolitica bioserotype 4/O:3. O:3 strains are highly prevalent in pigs, which are usually symptomless carriers, and they represent the most common cause of human yersiniosis. To assess the pathogenic potential of the O:3 serotype, we compared the colonization properties of Y. enterocolitica O:3 with O:8, a highly mouse-virulent Y. enterocolitica serotype, in minipigs and mice. We found ...[more]

PMID: 24343656

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Project description:BackgroundPigs are the most important reservoir for human pathogenic Yersinia enterocolitica. We investigated the herd prevalence of human pathogenic Y. enterocolitica in Swedish pig farms by analysing pen faecal samples using a cold enrichment of 1 week and thereafter subsequent plating onto chromogenic selective media (CAY agar).ResultsPathogenic Y. enterocolitica was found in 32 (30.5%) of the 105 sampled farms with finisher pigs. Bioserotype 4/O:3 was identified at all but one farm, where 2/O:9 was identified. Pen-prevalence within the positive herds varied from 1/4 to 4/4 pens. The calculated intra-class correlation coefficient ICC (0.89) from a model with a random effect for grouping within herd indicated a very high degree of clustering by herd. None of the explored risk factors, including herd size, herd type, pig flow, feed type, access to outdoors, evidence of birds and rodents in the herd, usage of straw, number of pigs in sampled pen and age of pigs in pen were significantly associated with Y. enterocolitica status of the pen. The use of high pressure washing with cold water was significantly associated with Y. enterocolitica in the pen (OR = 84.77, 4.05-1772). Two culture methods were assessed for detection of Y. enterocolitica, one of which included the use of a chromogenic agar (CAY agar) intended for detection of human pathogenic Y. enterocolitica. The chromogenic media was found equal or superior to traditional methods and was used in this study. The isolates obtained were characterised by biotyping, serotyping, mass spectrometry (MALDI-TOF) and PCR. Characterisation by MALDI-TOF gave identical results to that of conventional bioserotyping. All porcine isolates were positive for the ail and inv genes by PCR, indicating that the isolates were most likely pathogenic to humans.ConclusionsHuman pathogenic Y. enterocolitica was found in nearly one-third of the Swedish pig farms with finisher pigs. The use of high pressure washing with cold water was associated with the presence of Y. enterocolitica in the pen. A modified culturing method using a chromogenic agar was efficient for detection of pathogenic Y. enterocolitica in pig faeces. The use of masspectrometry for identification and subtyping was in agreement with conventional biotyping and serotyping methods.

Project description:BACKGROUND: Yersinia enterocolitica is a gastrointestinal foodborne pathogen found worldwide and which especially affects infants and young children. While different bioserotypes have been associated with varying pathogenicity, research on Y. enterocolitica is mainly conducted on the highly virulent mouse-lethal strains of biotype 1B and serotype O:8. We demonstrate here that two Y. enterocolitica bioserotype 1B/O:8 strains, 8081 and WA-314, display different virulence and fitness properties in a mouse model. In vivo co-infection experiments revealed that strain WA-314 overcomes strain 8081 in the colonization of spleen and liver. To trace the reasons of this incongruity, we present here the first high-quality sequence of the whole genome of strain WA-314 and compare it to the published genome of strain 8081. RESULTS: Regions previously accepted as unique to strain 8081, like the YAPI and YGI-3 genomic islands, are absent from strain WA-314, confirming their strain-specificity. On the other hand, some fitness- and bacterial competition-associated features, such as a putative colicin cluster and a xenobiotic-acyltransferase-encoding gene, are unique to strain WA-314. Additional acquisitions of strain WA-314 are seven prophage-like regions. One of these prophages, the 28-kb P4-like prophage YWA-4, encodes a PilV-like protein that may be used for adhesion to and invasion of the intestinal cells. Furthermore, a putative autotransporter and two type 1 fimbrial proteins of strain WA-314 show a sequence similarity <50% with the orthologous proteins in strain 8081. The dissimilar sequences of these proteins indicate possible different functions or interaction modes, reflecting the specific adhesion properties of Y. enterocolitica strains 8081 and WA-314 and thus the different efficiency of host colonization. Further important differences were found in two pYV plasmid-encoded virulence factors, YopM and YscP. The impact of these differences on virulence is discussed. CONCLUSIONS: Our study emphasizes that the virulence of pathogens can be increased, by acquiring new genes and/or improving the function of essential virulence proteins, resulting in permanently hyper-virulent strains. This work also highlights the importance of addressing genetic and phenotypic variations among closely related bacterial strains, even those belonging to the same bioserotype.

Dataset Information

Essential role of invasin for colonization and persistence of Yersinia enterocolitica in its natural reservoir host, the pig.

Publications

Essential role of invasin for colonization and persistence of Yersinia enterocolitica in its natural reservoir host, the pig.

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