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Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and Enteritidis.

Blondel CJ, Yang HJ, Castro B, Chiang S, Toro CS, Zaldívar M, Contreras I, Andrews-Polymenis HL, Santiviago CA - PLoS ONE (2010)

Bottom Line: Non-polar deletion mutants of SPI-19 and the clpV gene, an essential T6SS component, colonized the ileum, ceca, liver and spleen of White Leghorn chicks poorly compared to the wild-type strain after oral inoculation.In contrast, transfer of SPI-19 from Gallinarum to Enteritidis resulted in transient increase in the colonization of the ileum, liver and spleen at day 1 post-infection, but at days 3 and 5 post-infection a strong colonization defect of the gut and internal organs of the experimentally infected chickens was observed.Our data indicate that SPI-19 and the T6SS encoded in this region contribute to the colonization of the gastrointestinal tract and internal organs of chickens by Salmonella Gallinarum and suggest that degradation of SPI-19 T6SS in Salmonella Enteritidis conferred an advantage in colonization of the avian host.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Químicas y Farmacéuticas, Universidad de Chile, Santiago, Chile.

ABSTRACT
Salmonella Gallinarum is a pathogen with a host range specific to poultry, while Salmonella Enteritidis is a broad host range pathogen that colonizes poultry sub-clinically but is a leading cause of gastrointestinal salmonellosis in humans and many other species. Despite recent advances in our understanding of the complex interplay between Salmonella and their hosts, the molecular basis of host range restriction and unique pathobiology of Gallinarum remain largely unknown. Type VI Secretion System (T6SS) represents a new paradigm of protein secretion that is critical for the pathogenesis of many gram-negative bacteria. We recently identified a putative T6SS in the Salmonella Pathogenicity Island 19 (SPI-19) of Gallinarum. In Enteritidis, SPI-19 is a degenerate element that has lost most of the T6SS functions encoded in the island. In this work, we studied the contribution of SPI-19 to the colonization of Salmonella Gallinarum strain 287/91 in chickens. Non-polar deletion mutants of SPI-19 and the clpV gene, an essential T6SS component, colonized the ileum, ceca, liver and spleen of White Leghorn chicks poorly compared to the wild-type strain after oral inoculation. Return of SPI-19 to the DeltaSPI-19 mutant, using VEX-Capture, complemented this colonization defect. In contrast, transfer of SPI-19 from Gallinarum to Enteritidis resulted in transient increase in the colonization of the ileum, liver and spleen at day 1 post-infection, but at days 3 and 5 post-infection a strong colonization defect of the gut and internal organs of the experimentally infected chickens was observed. Our data indicate that SPI-19 and the T6SS encoded in this region contribute to the colonization of the gastrointestinal tract and internal organs of chickens by Salmonella Gallinarum and suggest that degradation of SPI-19 T6SS in Salmonella Enteritidis conferred an advantage in colonization of the avian host.

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Distribution of S. Gallinarum strain 287/91 in the gastrointestinal tract and internal organs of orally infected chickens.White Leghorn chicks were orally infected with ∼109 CFU of the wild-type S. Gallinarum 287/91 strain. After 1, 3 and 5 days post-infection the chicks were humanely euthanized, the ileum, ceca, liver and spleen were aseptically removed, tissues were homogenized and viable bacterial counts were determined. Data are mean values of log10 CFU/g of tissue, from four animals at each time point.
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pone-0011724-g002: Distribution of S. Gallinarum strain 287/91 in the gastrointestinal tract and internal organs of orally infected chickens.White Leghorn chicks were orally infected with ∼109 CFU of the wild-type S. Gallinarum 287/91 strain. After 1, 3 and 5 days post-infection the chicks were humanely euthanized, the ileum, ceca, liver and spleen were aseptically removed, tissues were homogenized and viable bacterial counts were determined. Data are mean values of log10 CFU/g of tissue, from four animals at each time point.

Mentions: Strain 287/91 is currently the only sequenced strain of serotype Gallinarum [5]. Although this isolate is reported to be highly virulent in susceptible chickens [5], there are no published reports regarding the systemic colonization dynamics of this strain in experimentally infected chickens. We infected White Leghorn chicks at four days of age with ∼1.39×109 CFU of the wild-type 287/91 strain by the oral route. The degree of colonization of the ileum, ceca, liver and spleen of infected chickens was determined at 1, 3 and 5 days post-infection (Figure 2). Strain 287/91 efficiently colonized the gut and internal organs of infected chicks from day 1 post-infection, gradually increasing during the remaining time points. At 5 days post infection the chicks were heavily colonized by S. Gallinarum but there were no noticeable differences in gross pathology with the uninfected control group and infected chicks did not show appreciable clinical signs of fowl typhoid. Nevertheless, since strain 287/91 efficiently colonized both the gut and internal organs of infected chickens, we used it to determine the contribution of SPI-19 to the colonization of chickens by S. Gallinarum.


Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and Enteritidis.

Blondel CJ, Yang HJ, Castro B, Chiang S, Toro CS, Zaldívar M, Contreras I, Andrews-Polymenis HL, Santiviago CA - PLoS ONE (2010)

Distribution of S. Gallinarum strain 287/91 in the gastrointestinal tract and internal organs of orally infected chickens.White Leghorn chicks were orally infected with ∼109 CFU of the wild-type S. Gallinarum 287/91 strain. After 1, 3 and 5 days post-infection the chicks were humanely euthanized, the ileum, ceca, liver and spleen were aseptically removed, tissues were homogenized and viable bacterial counts were determined. Data are mean values of log10 CFU/g of tissue, from four animals at each time point.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2908676&req=5

pone-0011724-g002: Distribution of S. Gallinarum strain 287/91 in the gastrointestinal tract and internal organs of orally infected chickens.White Leghorn chicks were orally infected with ∼109 CFU of the wild-type S. Gallinarum 287/91 strain. After 1, 3 and 5 days post-infection the chicks were humanely euthanized, the ileum, ceca, liver and spleen were aseptically removed, tissues were homogenized and viable bacterial counts were determined. Data are mean values of log10 CFU/g of tissue, from four animals at each time point.
Mentions: Strain 287/91 is currently the only sequenced strain of serotype Gallinarum [5]. Although this isolate is reported to be highly virulent in susceptible chickens [5], there are no published reports regarding the systemic colonization dynamics of this strain in experimentally infected chickens. We infected White Leghorn chicks at four days of age with ∼1.39×109 CFU of the wild-type 287/91 strain by the oral route. The degree of colonization of the ileum, ceca, liver and spleen of infected chickens was determined at 1, 3 and 5 days post-infection (Figure 2). Strain 287/91 efficiently colonized the gut and internal organs of infected chicks from day 1 post-infection, gradually increasing during the remaining time points. At 5 days post infection the chicks were heavily colonized by S. Gallinarum but there were no noticeable differences in gross pathology with the uninfected control group and infected chicks did not show appreciable clinical signs of fowl typhoid. Nevertheless, since strain 287/91 efficiently colonized both the gut and internal organs of infected chickens, we used it to determine the contribution of SPI-19 to the colonization of chickens by S. Gallinarum.

Bottom Line: Non-polar deletion mutants of SPI-19 and the clpV gene, an essential T6SS component, colonized the ileum, ceca, liver and spleen of White Leghorn chicks poorly compared to the wild-type strain after oral inoculation.In contrast, transfer of SPI-19 from Gallinarum to Enteritidis resulted in transient increase in the colonization of the ileum, liver and spleen at day 1 post-infection, but at days 3 and 5 post-infection a strong colonization defect of the gut and internal organs of the experimentally infected chickens was observed.Our data indicate that SPI-19 and the T6SS encoded in this region contribute to the colonization of the gastrointestinal tract and internal organs of chickens by Salmonella Gallinarum and suggest that degradation of SPI-19 T6SS in Salmonella Enteritidis conferred an advantage in colonization of the avian host.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Químicas y Farmacéuticas, Universidad de Chile, Santiago, Chile.

ABSTRACT
Salmonella Gallinarum is a pathogen with a host range specific to poultry, while Salmonella Enteritidis is a broad host range pathogen that colonizes poultry sub-clinically but is a leading cause of gastrointestinal salmonellosis in humans and many other species. Despite recent advances in our understanding of the complex interplay between Salmonella and their hosts, the molecular basis of host range restriction and unique pathobiology of Gallinarum remain largely unknown. Type VI Secretion System (T6SS) represents a new paradigm of protein secretion that is critical for the pathogenesis of many gram-negative bacteria. We recently identified a putative T6SS in the Salmonella Pathogenicity Island 19 (SPI-19) of Gallinarum. In Enteritidis, SPI-19 is a degenerate element that has lost most of the T6SS functions encoded in the island. In this work, we studied the contribution of SPI-19 to the colonization of Salmonella Gallinarum strain 287/91 in chickens. Non-polar deletion mutants of SPI-19 and the clpV gene, an essential T6SS component, colonized the ileum, ceca, liver and spleen of White Leghorn chicks poorly compared to the wild-type strain after oral inoculation. Return of SPI-19 to the DeltaSPI-19 mutant, using VEX-Capture, complemented this colonization defect. In contrast, transfer of SPI-19 from Gallinarum to Enteritidis resulted in transient increase in the colonization of the ileum, liver and spleen at day 1 post-infection, but at days 3 and 5 post-infection a strong colonization defect of the gut and internal organs of the experimentally infected chickens was observed. Our data indicate that SPI-19 and the T6SS encoded in this region contribute to the colonization of the gastrointestinal tract and internal organs of chickens by Salmonella Gallinarum and suggest that degradation of SPI-19 T6SS in Salmonella Enteritidis conferred an advantage in colonization of the avian host.

Show MeSH
Related in: MedlinePlus