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

Carlos J. Blondel, Hee Jeong Yang, Benjamín Castro, Sebastián Chiang, Cecilia S. Toro, Mercedes Zaldïvar, Inés Contreras, Helene L. Andrews-Polymenis, Carlos A. Santiviago

Resultado de la investigación: Article

46 Citas (Scopus)

Resumen

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 Gramnegative 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 DSPI-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.

Idioma originalEnglish
Número de artículoe11724
PublicaciónPLoS ONE
Volumen5
N.º7
DOI
EstadoPublished - 13 ago 2010

Huella dactilar

Salmonella Gallinarum
pathogenicity islands
Genomic Islands
Salmonella
Salmonella enterica
Chickens
chickens
Salmonella Enteritidis
host range
Host Specificity
ileum
Salmonella enteritidis
poultry
spleen
Poultry
Ileum
mutants
liver
Pathogens
protein secretion

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • General

Citar esto

Blondel, Carlos J. ; Yang, Hee Jeong ; Castro, Benjamín ; Chiang, Sebastián ; Toro, Cecilia S. ; Zaldïvar, Mercedes ; Contreras, Inés ; Andrews-Polymenis, Helene L. ; Santiviago, Carlos A. / Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and enteritidis. En: PLoS ONE. 2010 ; Vol. 5, N.º 7.
@article{4a3baa47baa24d95bb66a96eebcab8fe,
title = "Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and enteritidis",
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 Gramnegative 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 DSPI-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.",
author = "Blondel, {Carlos J.} and Yang, {Hee Jeong} and Benjam{\'i}n Castro and Sebasti{\'a}n Chiang and Toro, {Cecilia S.} and Mercedes Zald{\"i}var and In{\'e}s Contreras and Andrews-Polymenis, {Helene L.} and Santiviago, {Carlos A.}",
year = "2010",
month = "8",
day = "13",
doi = "10.1371/journal.pone.0011724",
language = "English",
volume = "5",
journal = "PLoS ONE",
issn = "1932-6203",
publisher = "Public Library of Science",
number = "7",

}

Blondel, CJ, Yang, HJ, Castro, B, Chiang, S, Toro, CS, Zaldïvar, M, Contreras, I, Andrews-Polymenis, HL & Santiviago, CA 2010, 'Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and enteritidis', PLoS ONE, vol. 5, n.º 7, e11724. https://doi.org/10.1371/journal.pone.0011724

Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and enteritidis. / Blondel, Carlos J.; Yang, Hee Jeong; Castro, Benjamín; Chiang, Sebastián; Toro, Cecilia S.; Zaldïvar, Mercedes; Contreras, Inés; Andrews-Polymenis, Helene L.; Santiviago, Carlos A.

En: PLoS ONE, Vol. 5, N.º 7, e11724, 13.08.2010.

Resultado de la investigación: Article

TY - JOUR

T1 - Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and enteritidis

AU - Blondel, Carlos J.

AU - Yang, Hee Jeong

AU - Castro, Benjamín

AU - Chiang, Sebastián

AU - Toro, Cecilia S.

AU - Zaldïvar, Mercedes

AU - Contreras, Inés

AU - Andrews-Polymenis, Helene L.

AU - Santiviago, Carlos A.

PY - 2010/8/13

Y1 - 2010/8/13

N2 - 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 Gramnegative 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 DSPI-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.

AB - 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 Gramnegative 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 DSPI-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.

UR - http://www.scopus.com/inward/record.url?scp=77955345904&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0011724

DO - 10.1371/journal.pone.0011724

M3 - Article

C2 - 20661437

AN - SCOPUS:77955345904

VL - 5

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 7

M1 - e11724

ER -