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Horizontal gene transfer of a ColV plasmid has resulted in a dominant avian clonal type of Salmonella enterica serovar Kentucky.

Johnson TJ, Thorsness JL, Anderson CP, Lynne AM, Foley SL, Han J, Fricke WF, McDermott PF, White DG, Khatri M, Stell AL, Flores C, Singer RS - PLoS ONE (2010)

Bottom Line: Of the serovars examined, the ColV plasmid was found only among isolates belonging to the serovars Kentucky (72.9%), Typhimurium (15.0%) and Heidelberg (1.7%).Kentucky significantly increased its ability to colonize the chicken cecum and cause extraintestinal disease.Thus, the potential for horizontal gene transfer of virulence and fitness factors to Salmonella from other enteric bacteria exists in poultry, representing a potential human health hazard.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary and Biomedical Sciences, University of Minnesota, St Paul, Minnesota, United States of America. joh04207@umn.edu

ABSTRACT
Salmonella enterica continues to be a significant cause of foodborne gastrointestinal illness in humans. A wide variety of Salmonella serovars have been isolated from production birds and from retail poultry meat. Recently, though, S. enterica subsp. enterica serovar Kentucky has emerged as one of the prominent Salmonella serovars isolated from broiler chickens. Recent work suggests that its emergence apparently coincides with its acquisition of a ColV virulence plasmid. In the present study, we examined 902 Salmonella isolates belonging to 59 different serovars for the presence of this plasmid. Of the serovars examined, the ColV plasmid was found only among isolates belonging to the serovars Kentucky (72.9%), Typhimurium (15.0%) and Heidelberg (1.7%). We demonstrated that a single PFGE clonal type of S. Kentucky harbors this plasmid, and acquisition of this plasmid by S. Kentucky significantly increased its ability to colonize the chicken cecum and cause extraintestinal disease. Comparison of the completed sequences of three ColV plasmids from S. Kentucky isolated from different geographical locales, timepoints and sources revealed a nearly identical genetic structure with few single nucleotide changes or insertions/deletions. Overall, it appears that the ColV plasmid was recently acquired by a single clonal type S. Kentucky and confers to its host enhanced colonization and fitness capabilities. Thus, the potential for horizontal gene transfer of virulence and fitness factors to Salmonella from other enteric bacteria exists in poultry, representing a potential human health hazard.

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Chicken competition colonization model using plasmid-containing and plasmid-lacking strains.(A) competes plasmid-containing and plasmid lacking S. Kentucky CVM35942; (B) competes plasmid-containing and plasmid lacking S. Kentucky CVM29188; (C) competes S. Kentucky CVM35942p with S. Newport SL317. Competition Index (CI) values are presented so that a CI value >1 means that strain 1 outcompeted strain 2, and a CI value <1 means that strain 2 outcompeted strain 1. P values shown below Day were calculated relative to 1 using a Student's t-test. Strains with “p” refer to the transconjugant of a strain containing pCVM29188_146, while strains with “c” refer to a wild type strain cured of its ColV plasmid.
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pone-0015524-g004: Chicken competition colonization model using plasmid-containing and plasmid-lacking strains.(A) competes plasmid-containing and plasmid lacking S. Kentucky CVM35942; (B) competes plasmid-containing and plasmid lacking S. Kentucky CVM29188; (C) competes S. Kentucky CVM35942p with S. Newport SL317. Competition Index (CI) values are presented so that a CI value >1 means that strain 1 outcompeted strain 2, and a CI value <1 means that strain 2 outcompeted strain 1. P values shown below Day were calculated relative to 1 using a Student's t-test. Strains with “p” refer to the transconjugant of a strain containing pCVM29188_146, while strains with “c” refer to a wild type strain cured of its ColV plasmid.

Mentions: A collection of ColV plasmid-containing and plasmid-lacking Salmonella isolates (Table 3) was used to test their abilities to colonize specific-pathogen-free (SPF) chickens. The isolates were compared in a relative colonization model (Fig. 3) and a competition model (Fig. 4). In the relative colonization model, plasmidless S. Kentucky strain 35942 belonging to the chicken PFGE profile was compared to its ColV plasmid-containing transconjugant. Similarly, S. Newport strain SL317, a human isolate, was compared to its ColV plasmid-containing transconjugant. For comparison purposes, two additional ColV+ wild type S. Kentucky strains from broiler chickens (CS0010-A and SSAP03302-A) were also compared, both belonging to the chicken PFGE profile. On all days sampled over a two-week period post-inoculation, plasmid-containing strain CVM35942p colonized significantly better (p<0.05) than its plasmid-lacking counterpart. CVM35942p also colonized at similar levels to the other wild type ColV+ S. Kentucky strains belonging to the same chicken PFGE profile. These plasmid-containing S. Kentucky strains colonized significantly better (p<0.05) than either of the S. Newport strains tested. The S. Newport strain SL317p containing the ColV plasmid colonized better than plasmid-lacking SL317 at all timepoints, but these differences were not statistically significant. Spleen tissues were also cultured from all birds tested, but no bacteria were recovered in any of the samples (data not shown).


Horizontal gene transfer of a ColV plasmid has resulted in a dominant avian clonal type of Salmonella enterica serovar Kentucky.

Johnson TJ, Thorsness JL, Anderson CP, Lynne AM, Foley SL, Han J, Fricke WF, McDermott PF, White DG, Khatri M, Stell AL, Flores C, Singer RS - PLoS ONE (2010)

Chicken competition colonization model using plasmid-containing and plasmid-lacking strains.(A) competes plasmid-containing and plasmid lacking S. Kentucky CVM35942; (B) competes plasmid-containing and plasmid lacking S. Kentucky CVM29188; (C) competes S. Kentucky CVM35942p with S. Newport SL317. Competition Index (CI) values are presented so that a CI value >1 means that strain 1 outcompeted strain 2, and a CI value <1 means that strain 2 outcompeted strain 1. P values shown below Day were calculated relative to 1 using a Student's t-test. Strains with “p” refer to the transconjugant of a strain containing pCVM29188_146, while strains with “c” refer to a wild type strain cured of its ColV plasmid.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3008734&req=5

pone-0015524-g004: Chicken competition colonization model using plasmid-containing and plasmid-lacking strains.(A) competes plasmid-containing and plasmid lacking S. Kentucky CVM35942; (B) competes plasmid-containing and plasmid lacking S. Kentucky CVM29188; (C) competes S. Kentucky CVM35942p with S. Newport SL317. Competition Index (CI) values are presented so that a CI value >1 means that strain 1 outcompeted strain 2, and a CI value <1 means that strain 2 outcompeted strain 1. P values shown below Day were calculated relative to 1 using a Student's t-test. Strains with “p” refer to the transconjugant of a strain containing pCVM29188_146, while strains with “c” refer to a wild type strain cured of its ColV plasmid.
Mentions: A collection of ColV plasmid-containing and plasmid-lacking Salmonella isolates (Table 3) was used to test their abilities to colonize specific-pathogen-free (SPF) chickens. The isolates were compared in a relative colonization model (Fig. 3) and a competition model (Fig. 4). In the relative colonization model, plasmidless S. Kentucky strain 35942 belonging to the chicken PFGE profile was compared to its ColV plasmid-containing transconjugant. Similarly, S. Newport strain SL317, a human isolate, was compared to its ColV plasmid-containing transconjugant. For comparison purposes, two additional ColV+ wild type S. Kentucky strains from broiler chickens (CS0010-A and SSAP03302-A) were also compared, both belonging to the chicken PFGE profile. On all days sampled over a two-week period post-inoculation, plasmid-containing strain CVM35942p colonized significantly better (p<0.05) than its plasmid-lacking counterpart. CVM35942p also colonized at similar levels to the other wild type ColV+ S. Kentucky strains belonging to the same chicken PFGE profile. These plasmid-containing S. Kentucky strains colonized significantly better (p<0.05) than either of the S. Newport strains tested. The S. Newport strain SL317p containing the ColV plasmid colonized better than plasmid-lacking SL317 at all timepoints, but these differences were not statistically significant. Spleen tissues were also cultured from all birds tested, but no bacteria were recovered in any of the samples (data not shown).

Bottom Line: Of the serovars examined, the ColV plasmid was found only among isolates belonging to the serovars Kentucky (72.9%), Typhimurium (15.0%) and Heidelberg (1.7%).Kentucky significantly increased its ability to colonize the chicken cecum and cause extraintestinal disease.Thus, the potential for horizontal gene transfer of virulence and fitness factors to Salmonella from other enteric bacteria exists in poultry, representing a potential human health hazard.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary and Biomedical Sciences, University of Minnesota, St Paul, Minnesota, United States of America. joh04207@umn.edu

ABSTRACT
Salmonella enterica continues to be a significant cause of foodborne gastrointestinal illness in humans. A wide variety of Salmonella serovars have been isolated from production birds and from retail poultry meat. Recently, though, S. enterica subsp. enterica serovar Kentucky has emerged as one of the prominent Salmonella serovars isolated from broiler chickens. Recent work suggests that its emergence apparently coincides with its acquisition of a ColV virulence plasmid. In the present study, we examined 902 Salmonella isolates belonging to 59 different serovars for the presence of this plasmid. Of the serovars examined, the ColV plasmid was found only among isolates belonging to the serovars Kentucky (72.9%), Typhimurium (15.0%) and Heidelberg (1.7%). We demonstrated that a single PFGE clonal type of S. Kentucky harbors this plasmid, and acquisition of this plasmid by S. Kentucky significantly increased its ability to colonize the chicken cecum and cause extraintestinal disease. Comparison of the completed sequences of three ColV plasmids from S. Kentucky isolated from different geographical locales, timepoints and sources revealed a nearly identical genetic structure with few single nucleotide changes or insertions/deletions. Overall, it appears that the ColV plasmid was recently acquired by a single clonal type S. Kentucky and confers to its host enhanced colonization and fitness capabilities. Thus, the potential for horizontal gene transfer of virulence and fitness factors to Salmonella from other enteric bacteria exists in poultry, representing a potential human health hazard.

Show MeSH
Related in: MedlinePlus