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A reservoir of drug-resistant pathogenic bacteria in asymptomatic hosts.

Perron GG, Quessy S, Bell G - PLoS ONE (2008)

Bottom Line: However, much less attention has been paid to bacterial carriage populations, which inhabit hosts without producing disease.We have found that asymptomatic swine from livestock productions frequently carry populations of Salmonella enterica with a broad range of drug-resistant strains and genetic diversity greatly exceeding that previously described.This study shows how agricultural practice and human intervention may lead and influence the evolution of a hidden reservoir of pathogens, with important implications for human health.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, McGill University, Montreal, Quebec, Canada. gabriel.guimond-perron@zoo.ox.ac.uk

ABSTRACT
The population genetics of pathogenic bacteria has been intensively studied in order to understand the spread of disease and the evolution of virulence and drug resistance. However, much less attention has been paid to bacterial carriage populations, which inhabit hosts without producing disease. Since new virulent strains that cause disease can be recruited from the carriage population of bacteria, our understanding of infectious disease is seriously incomplete without knowledge on the population structure of pathogenic bacteria living in an asymptomatic host. We report the first extensive survey of the abundance and diversity of a human pathogen in asymptomatic animal hosts. We have found that asymptomatic swine from livestock productions frequently carry populations of Salmonella enterica with a broad range of drug-resistant strains and genetic diversity greatly exceeding that previously described. This study shows how agricultural practice and human intervention may lead and influence the evolution of a hidden reservoir of pathogens, with important implications for human health.

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Maximum likelihood tree representing the twenty sequence types associated with asymptomatic swine.The number of isolates (in brackets) and the percentage of the most frequent serotype are shown.
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pone-0003749-g003: Maximum likelihood tree representing the twenty sequence types associated with asymptomatic swine.The number of isolates (in brackets) and the percentage of the most frequent serotype are shown.

Mentions: We then examined the population structure and underlying genetic variation in our sample using the nucleotide sequences of seven housekeeping loci analysed by multilocus sequence typing (MLST). We identified 20 genotypes, with most falling into two clonal groups as defined by an eBURST analysis (Figure 3). We found that there was very little genetic recombination. The overall mean recombination rate was 5.4×10−4 per locus, with any given nucleotide being about 15 times more likely to be changed by mutation as by recombination (see Table S4). Hence, Salmonella from asymptomatic infections has a nearly completely clonal structure, as has been previously established for virulent strains [29]. However, while previous investigations of Salmonella population structure found little genetic variability over years [30], [31]or among disease-associated stains of different host origin [32], we discovered six new genotypes of DT104 among asymptomatic isolates. Furthermore, this diversity was sampled in a single host species over a period of a few weeks, and hence does not include temporal variation. Because of the clonal nature of Salmonella, most of the variation observed, and therefore the adaptation of the bacterium, would be transmitted vertically from novel mutations. Interestingly, the majority of the antibiotic-resistant and multidrug-resistant phenotypes were associated with this emergent diverse group of Salmonella DT104 strains. Although, antibiotic resistance can be transmitted horizontally in bacteria such as Salmonella [33]–[36], it has been previously demonstrated that the capability to exchange such genetic material is restricted to certain lineages [37]. Thus, it appears that despite some level of horizontal transfer among closely related strains, the distribution of traits (like antibiotic resistance) is clonally distributed and mainly affected by the evolution within clonal group.


A reservoir of drug-resistant pathogenic bacteria in asymptomatic hosts.

Perron GG, Quessy S, Bell G - PLoS ONE (2008)

Maximum likelihood tree representing the twenty sequence types associated with asymptomatic swine.The number of isolates (in brackets) and the percentage of the most frequent serotype are shown.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2581806&req=5

pone-0003749-g003: Maximum likelihood tree representing the twenty sequence types associated with asymptomatic swine.The number of isolates (in brackets) and the percentage of the most frequent serotype are shown.
Mentions: We then examined the population structure and underlying genetic variation in our sample using the nucleotide sequences of seven housekeeping loci analysed by multilocus sequence typing (MLST). We identified 20 genotypes, with most falling into two clonal groups as defined by an eBURST analysis (Figure 3). We found that there was very little genetic recombination. The overall mean recombination rate was 5.4×10−4 per locus, with any given nucleotide being about 15 times more likely to be changed by mutation as by recombination (see Table S4). Hence, Salmonella from asymptomatic infections has a nearly completely clonal structure, as has been previously established for virulent strains [29]. However, while previous investigations of Salmonella population structure found little genetic variability over years [30], [31]or among disease-associated stains of different host origin [32], we discovered six new genotypes of DT104 among asymptomatic isolates. Furthermore, this diversity was sampled in a single host species over a period of a few weeks, and hence does not include temporal variation. Because of the clonal nature of Salmonella, most of the variation observed, and therefore the adaptation of the bacterium, would be transmitted vertically from novel mutations. Interestingly, the majority of the antibiotic-resistant and multidrug-resistant phenotypes were associated with this emergent diverse group of Salmonella DT104 strains. Although, antibiotic resistance can be transmitted horizontally in bacteria such as Salmonella [33]–[36], it has been previously demonstrated that the capability to exchange such genetic material is restricted to certain lineages [37]. Thus, it appears that despite some level of horizontal transfer among closely related strains, the distribution of traits (like antibiotic resistance) is clonally distributed and mainly affected by the evolution within clonal group.

Bottom Line: However, much less attention has been paid to bacterial carriage populations, which inhabit hosts without producing disease.We have found that asymptomatic swine from livestock productions frequently carry populations of Salmonella enterica with a broad range of drug-resistant strains and genetic diversity greatly exceeding that previously described.This study shows how agricultural practice and human intervention may lead and influence the evolution of a hidden reservoir of pathogens, with important implications for human health.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, McGill University, Montreal, Quebec, Canada. gabriel.guimond-perron@zoo.ox.ac.uk

ABSTRACT
The population genetics of pathogenic bacteria has been intensively studied in order to understand the spread of disease and the evolution of virulence and drug resistance. However, much less attention has been paid to bacterial carriage populations, which inhabit hosts without producing disease. Since new virulent strains that cause disease can be recruited from the carriage population of bacteria, our understanding of infectious disease is seriously incomplete without knowledge on the population structure of pathogenic bacteria living in an asymptomatic host. We report the first extensive survey of the abundance and diversity of a human pathogen in asymptomatic animal hosts. We have found that asymptomatic swine from livestock productions frequently carry populations of Salmonella enterica with a broad range of drug-resistant strains and genetic diversity greatly exceeding that previously described. This study shows how agricultural practice and human intervention may lead and influence the evolution of a hidden reservoir of pathogens, with important implications for human health.

Show MeSH
Related in: MedlinePlus