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Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens.

Rychlik I, Karasova D, Sebkova A, Volf J, Sisak F, Havlickova H, Kummer V, Imre A, Szmolka A, Nagy B - BMC Microbiol. (2009)

Bottom Line: Salmonella is a highly successful parasite of reptiles, birds and mammals.In contrast, the absence of SPI-3, SPI-4 or SPI-5 individually did not influence virulence of S.SPI-1 and SPI-2 are the two most important pathogenicity islands of Salmonella Enteritidis required for the colonisation of systemic sites in chickens.

View Article: PubMed Central - HTML - PubMed

Affiliation: Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic. rychlik@vri.cz

ABSTRACT

Background: Salmonella is a highly successful parasite of reptiles, birds and mammals. Its ability to infect and colonise such a broad range of hosts coincided with the introduction of new genetic determinants, among them 5 major pathogenicity islands (SPI1-5), into the Salmonella genome. However, only limited information is available on how each of these pathogenicity islands influences the ability of Salmonella to infect chickens. In this study, we therefore constructed Salmonella Enteritidis mutants with each SPI deleted separately, with single individual SPIs (i.e. with the remaining four deleted) and a mutant with all 5 SPIs deleted, and assessed their virulence in one-day-old chickens, together with the innate immune response of this host.

Results: The mutant lacking all 5 major SPIs was still capable of colonising the caecum while colonisation of the liver and spleen was dependent on the presence of both SPI-1 and SPI-2. In contrast, the absence of SPI-3, SPI-4 or SPI-5 individually did not influence virulence of S. Enteritidis for chickens, but collectively they contributed to the colonisation of the spleen. Proinflammatory signalling and heterophil infiltration was dependent on intact SPI-1 only and not on other SPIs.

Conclusions: SPI-1 and SPI-2 are the two most important pathogenicity islands of Salmonella Enteritidis required for the colonisation of systemic sites in chickens.

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Distribution of S. Enteritidis 147 wild-type strain and SPI mutants in the spleen of orally infected chickens. S. Enteritidis counts in the liver correlated with counts in the spleen except for the fact that ΔSPI2 mutant colonised liver significantly less efficiently than the wild type S. Enteritidis also on day 12 (not shown). Y axis, average log CFU/g of spleen ± SD. a, b - ANOVA different at p < 0.05 in comparison to the group infected with the wild-type S. Enteritidis (a) or ΔSPI1-5 mutant (b). Abbreviations: wt - wild-type S. Enteritidis 147; ΔSPI1-5: mutant from which all major 5 SPI have been removed, ΔSPI1, ΔSPI2, ΔSPI3, ΔSPI4, ΔSPI5: mutants from which the respective SPI has been removed, SPI1o, SPI2o, SPI3o, SPI4o, SPI5o: "SPIonly" mutants, mutants with only the respective SPI retained.
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Figure 1: Distribution of S. Enteritidis 147 wild-type strain and SPI mutants in the spleen of orally infected chickens. S. Enteritidis counts in the liver correlated with counts in the spleen except for the fact that ΔSPI2 mutant colonised liver significantly less efficiently than the wild type S. Enteritidis also on day 12 (not shown). Y axis, average log CFU/g of spleen ± SD. a, b - ANOVA different at p < 0.05 in comparison to the group infected with the wild-type S. Enteritidis (a) or ΔSPI1-5 mutant (b). Abbreviations: wt - wild-type S. Enteritidis 147; ΔSPI1-5: mutant from which all major 5 SPI have been removed, ΔSPI1, ΔSPI2, ΔSPI3, ΔSPI4, ΔSPI5: mutants from which the respective SPI has been removed, SPI1o, SPI2o, SPI3o, SPI4o, SPI5o: "SPIonly" mutants, mutants with only the respective SPI retained.

Mentions: Both on day 5 and day 12, no significant differences in caecal colonisation were observed amongst all the mutants (data not shown). When the ability to persist in internal organs was analysed, the mutants could be clustered into 3 different groups as summarised in Table 1. The first group consisted of the wild-type strain and the ΔSPI3, ΔSPI4 and ΔSPI5 mutants. These strains colonised the liver and spleen with equal efficiency. The second group was formed by ΔSPI1-5, and the SPI3o, SPI4o and SPI5o mutants characterised by their inability to reach and persist in the liver and spleen of chickens. The last group was formed by ΔSPI1, ΔSPI2, and the SPI1o and SPI2o mutants which exhibited an intermediate ability to persist in liver and spleen of infected chickens (Fig. 1).


Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens.

Rychlik I, Karasova D, Sebkova A, Volf J, Sisak F, Havlickova H, Kummer V, Imre A, Szmolka A, Nagy B - BMC Microbiol. (2009)

Distribution of S. Enteritidis 147 wild-type strain and SPI mutants in the spleen of orally infected chickens. S. Enteritidis counts in the liver correlated with counts in the spleen except for the fact that ΔSPI2 mutant colonised liver significantly less efficiently than the wild type S. Enteritidis also on day 12 (not shown). Y axis, average log CFU/g of spleen ± SD. a, b - ANOVA different at p < 0.05 in comparison to the group infected with the wild-type S. Enteritidis (a) or ΔSPI1-5 mutant (b). Abbreviations: wt - wild-type S. Enteritidis 147; ΔSPI1-5: mutant from which all major 5 SPI have been removed, ΔSPI1, ΔSPI2, ΔSPI3, ΔSPI4, ΔSPI5: mutants from which the respective SPI has been removed, SPI1o, SPI2o, SPI3o, SPI4o, SPI5o: "SPIonly" mutants, mutants with only the respective SPI retained.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2803193&req=5

Figure 1: Distribution of S. Enteritidis 147 wild-type strain and SPI mutants in the spleen of orally infected chickens. S. Enteritidis counts in the liver correlated with counts in the spleen except for the fact that ΔSPI2 mutant colonised liver significantly less efficiently than the wild type S. Enteritidis also on day 12 (not shown). Y axis, average log CFU/g of spleen ± SD. a, b - ANOVA different at p < 0.05 in comparison to the group infected with the wild-type S. Enteritidis (a) or ΔSPI1-5 mutant (b). Abbreviations: wt - wild-type S. Enteritidis 147; ΔSPI1-5: mutant from which all major 5 SPI have been removed, ΔSPI1, ΔSPI2, ΔSPI3, ΔSPI4, ΔSPI5: mutants from which the respective SPI has been removed, SPI1o, SPI2o, SPI3o, SPI4o, SPI5o: "SPIonly" mutants, mutants with only the respective SPI retained.
Mentions: Both on day 5 and day 12, no significant differences in caecal colonisation were observed amongst all the mutants (data not shown). When the ability to persist in internal organs was analysed, the mutants could be clustered into 3 different groups as summarised in Table 1. The first group consisted of the wild-type strain and the ΔSPI3, ΔSPI4 and ΔSPI5 mutants. These strains colonised the liver and spleen with equal efficiency. The second group was formed by ΔSPI1-5, and the SPI3o, SPI4o and SPI5o mutants characterised by their inability to reach and persist in the liver and spleen of chickens. The last group was formed by ΔSPI1, ΔSPI2, and the SPI1o and SPI2o mutants which exhibited an intermediate ability to persist in liver and spleen of infected chickens (Fig. 1).

Bottom Line: Salmonella is a highly successful parasite of reptiles, birds and mammals.In contrast, the absence of SPI-3, SPI-4 or SPI-5 individually did not influence virulence of S.SPI-1 and SPI-2 are the two most important pathogenicity islands of Salmonella Enteritidis required for the colonisation of systemic sites in chickens.

View Article: PubMed Central - HTML - PubMed

Affiliation: Veterinary Research Institute, Hudcova 70, 621 00 Brno, Czech Republic. rychlik@vri.cz

ABSTRACT

Background: Salmonella is a highly successful parasite of reptiles, birds and mammals. Its ability to infect and colonise such a broad range of hosts coincided with the introduction of new genetic determinants, among them 5 major pathogenicity islands (SPI1-5), into the Salmonella genome. However, only limited information is available on how each of these pathogenicity islands influences the ability of Salmonella to infect chickens. In this study, we therefore constructed Salmonella Enteritidis mutants with each SPI deleted separately, with single individual SPIs (i.e. with the remaining four deleted) and a mutant with all 5 SPIs deleted, and assessed their virulence in one-day-old chickens, together with the innate immune response of this host.

Results: The mutant lacking all 5 major SPIs was still capable of colonising the caecum while colonisation of the liver and spleen was dependent on the presence of both SPI-1 and SPI-2. In contrast, the absence of SPI-3, SPI-4 or SPI-5 individually did not influence virulence of S. Enteritidis for chickens, but collectively they contributed to the colonisation of the spleen. Proinflammatory signalling and heterophil infiltration was dependent on intact SPI-1 only and not on other SPIs.

Conclusions: SPI-1 and SPI-2 are the two most important pathogenicity islands of Salmonella Enteritidis required for the colonisation of systemic sites in chickens.

Show MeSH
Related in: MedlinePlus