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Excision of an unstable pathogenicity island in Salmonella enterica serovar Enteritidis is induced during infection of phagocytic cells.

Quiroz TS, Nieto PA, Tobar HE, Salazar-Echegarai FJ, Lizana RJ, Quezada CP, Santiviago CA, Araya DV, Riedel CA, Kalergis AM, Bueno SM - PLoS ONE (2011)

Bottom Line: Importantly, we also found that one type of excision occurred at higher rates when S.Enteritidis was residing inside murine phagocytic cells.These data suggest that ROD21 is an unstable pathogenicity island, whose frequency of excision depends on the environmental conditions found inside phagocytic cells.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Millennium Institute on Immunology and Immunotherapy, Pontificia Universidad Católica de Chile, Santiago, Chile.

ABSTRACT
The availability of the complete genome sequence of several Salmonella enterica serovars has revealed the presence of unstable genetic elements in these bacteria, such as pathogenicity islands and prophages. This is the case of Salmonella enterica serovar Enteritidis (S. Enteritidis), a bacterium that causes gastroenteritis in humans and systemic infection in mice. The whole genome sequence analysis for S. Enteritidis unveiled the presence of several genetic regions that are absent in other Salmonella serovars. These regions have been denominated "regions of difference" (ROD). In this study we show that ROD21, one of such regions, behaves as an unstable pathogenicity island. We observed that ROD21 undergoes spontaneous excision by two independent recombination events, either under laboratory growth conditions or during infection of murine cells. Importantly, we also found that one type of excision occurred at higher rates when S. Enteritidis was residing inside murine phagocytic cells. These data suggest that ROD21 is an unstable pathogenicity island, whose frequency of excision depends on the environmental conditions found inside phagocytic cells.

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Schematic representation of ROD21 in the chromosome of S. Enteritidis.(A) Representation of the genetic location of the genes coding for the asparagine tRNA (asnT-1, -2 and -3) in the chromosome of S. Typhimurium and S. Enteritidis and the exact location of ROD21 in the chromosome of S. Enteritidis. Black and dark gray arrows represent those genes shared between both serovars and light gray arrows represent genes found only in ROD21 of S. Enteritidis. Numbers next to each scheme are coordinates in the chromosome of S. Typhimurium and S. Enteritidis. DRS stand for Direct Repeated Sequence (attR). (B) The alignments of DRS and asnT-1, asnT-2 (attL) and asnT-3 show that the DRS is identical to the last 22 bp of the asnT genes.
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pone-0026031-g001: Schematic representation of ROD21 in the chromosome of S. Enteritidis.(A) Representation of the genetic location of the genes coding for the asparagine tRNA (asnT-1, -2 and -3) in the chromosome of S. Typhimurium and S. Enteritidis and the exact location of ROD21 in the chromosome of S. Enteritidis. Black and dark gray arrows represent those genes shared between both serovars and light gray arrows represent genes found only in ROD21 of S. Enteritidis. Numbers next to each scheme are coordinates in the chromosome of S. Typhimurium and S. Enteritidis. DRS stand for Direct Repeated Sequence (attR). (B) The alignments of DRS and asnT-1, asnT-2 (attL) and asnT-3 show that the DRS is identical to the last 22 bp of the asnT genes.

Mentions: ROD21 is a 26,687 bp DNA fragment located between coordinates 2,061,170 and 2,087,657 in the S. Enteritidis PT4 NCTC13349 genome. ROD21 is found in a region of the S. Enteritidis chromosome that is common to the genome of S. Typhimurium strains LT2 and 14028 (Fig. 1A). ROD21 is found next to an asparagine tRNA gene (asnT-2 or attL) and at its right end is delimited by 24 base pairs (bp), 22 of which are identical to the 3′ end of asnT (Fig. 1B). This element was denominated direct repeated sequence (DRS or attR). Furthermore, near ROD21 there are other two asparagine tRNA genes located in the same orientation as asnT-2 (asnT-1 and asnT-3 in this study). asnT-1 is located 971 bp upstream of asnT-2, while asnT-3 is located 11,487 bp downstream of the DRS. A fourth asparagine tRNA gene (asnW) is located 9,943 pb downstream of the DRS, but in the opposite direction when compared to the other asnT genes.


Excision of an unstable pathogenicity island in Salmonella enterica serovar Enteritidis is induced during infection of phagocytic cells.

Quiroz TS, Nieto PA, Tobar HE, Salazar-Echegarai FJ, Lizana RJ, Quezada CP, Santiviago CA, Araya DV, Riedel CA, Kalergis AM, Bueno SM - PLoS ONE (2011)

Schematic representation of ROD21 in the chromosome of S. Enteritidis.(A) Representation of the genetic location of the genes coding for the asparagine tRNA (asnT-1, -2 and -3) in the chromosome of S. Typhimurium and S. Enteritidis and the exact location of ROD21 in the chromosome of S. Enteritidis. Black and dark gray arrows represent those genes shared between both serovars and light gray arrows represent genes found only in ROD21 of S. Enteritidis. Numbers next to each scheme are coordinates in the chromosome of S. Typhimurium and S. Enteritidis. DRS stand for Direct Repeated Sequence (attR). (B) The alignments of DRS and asnT-1, asnT-2 (attL) and asnT-3 show that the DRS is identical to the last 22 bp of the asnT genes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3198454&req=5

pone-0026031-g001: Schematic representation of ROD21 in the chromosome of S. Enteritidis.(A) Representation of the genetic location of the genes coding for the asparagine tRNA (asnT-1, -2 and -3) in the chromosome of S. Typhimurium and S. Enteritidis and the exact location of ROD21 in the chromosome of S. Enteritidis. Black and dark gray arrows represent those genes shared between both serovars and light gray arrows represent genes found only in ROD21 of S. Enteritidis. Numbers next to each scheme are coordinates in the chromosome of S. Typhimurium and S. Enteritidis. DRS stand for Direct Repeated Sequence (attR). (B) The alignments of DRS and asnT-1, asnT-2 (attL) and asnT-3 show that the DRS is identical to the last 22 bp of the asnT genes.
Mentions: ROD21 is a 26,687 bp DNA fragment located between coordinates 2,061,170 and 2,087,657 in the S. Enteritidis PT4 NCTC13349 genome. ROD21 is found in a region of the S. Enteritidis chromosome that is common to the genome of S. Typhimurium strains LT2 and 14028 (Fig. 1A). ROD21 is found next to an asparagine tRNA gene (asnT-2 or attL) and at its right end is delimited by 24 base pairs (bp), 22 of which are identical to the 3′ end of asnT (Fig. 1B). This element was denominated direct repeated sequence (DRS or attR). Furthermore, near ROD21 there are other two asparagine tRNA genes located in the same orientation as asnT-2 (asnT-1 and asnT-3 in this study). asnT-1 is located 971 bp upstream of asnT-2, while asnT-3 is located 11,487 bp downstream of the DRS. A fourth asparagine tRNA gene (asnW) is located 9,943 pb downstream of the DRS, but in the opposite direction when compared to the other asnT genes.

Bottom Line: Importantly, we also found that one type of excision occurred at higher rates when S.Enteritidis was residing inside murine phagocytic cells.These data suggest that ROD21 is an unstable pathogenicity island, whose frequency of excision depends on the environmental conditions found inside phagocytic cells.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Genética Molecular y Microbiología, Facultad de Ciencias Biológicas, Millennium Institute on Immunology and Immunotherapy, Pontificia Universidad Católica de Chile, Santiago, Chile.

ABSTRACT
The availability of the complete genome sequence of several Salmonella enterica serovars has revealed the presence of unstable genetic elements in these bacteria, such as pathogenicity islands and prophages. This is the case of Salmonella enterica serovar Enteritidis (S. Enteritidis), a bacterium that causes gastroenteritis in humans and systemic infection in mice. The whole genome sequence analysis for S. Enteritidis unveiled the presence of several genetic regions that are absent in other Salmonella serovars. These regions have been denominated "regions of difference" (ROD). In this study we show that ROD21, one of such regions, behaves as an unstable pathogenicity island. We observed that ROD21 undergoes spontaneous excision by two independent recombination events, either under laboratory growth conditions or during infection of murine cells. Importantly, we also found that one type of excision occurred at higher rates when S. Enteritidis was residing inside murine phagocytic cells. These data suggest that ROD21 is an unstable pathogenicity island, whose frequency of excision depends on the environmental conditions found inside phagocytic cells.

Show MeSH
Related in: MedlinePlus