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Genomic Comparison of Non-Typhoidal Salmonella enterica Serovars Typhimurium, Enteritidis, Heidelberg, Hadar and Kentucky Isolates from Broiler Chickens.

Dhanani AS, Block G, Dewar K, Forgetta V, Topp E, Beiko RG, Diarra MS - PLoS ONE (2015)

Bottom Line: The colonization of the chicken gut by S. enterica could result in the contamination of the environment and food chain.Genes associated with the IncF plasmid and the IncI1 plasmid were identified in twelve and four isolates, respectively, while genes associated with the IncQ plasmid were found in one isolate.The presence of numerous genes associated with Salmonella pathogenicity islands (SPIs) was also confirmed.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Computer Science, Dalhousie University, Halifax, Nova Scotia, B3H 4R2, Canada.

ABSTRACT

Background: Non-typhoidal Salmonella enterica serovars, associated with different foods including poultry products, are important causes of bacterial gastroenteritis worldwide. The colonization of the chicken gut by S. enterica could result in the contamination of the environment and food chain. The aim of this study was to compare the genomes of 25 S. enterica serovars isolated from broiler chicken farms to assess their intra- and inter-genetic variability, with a focus on virulence and antibiotic resistance characteristics.

Methodology/principal finding: The genomes of 25 S. enterica isolates covering five serovars (ten Typhimurium including three monophasic 4,[5],12:i:, four Enteritidis, three Hadar, four Heidelberg and four Kentucky) were sequenced. Most serovars were clustered in strongly supported phylogenetic clades, except for isolates of serovar Enteritidis that were scattered throughout the tree. Plasmids of varying sizes were detected in several isolates independently of serovars. Genes associated with the IncF plasmid and the IncI1 plasmid were identified in twelve and four isolates, respectively, while genes associated with the IncQ plasmid were found in one isolate. The presence of numerous genes associated with Salmonella pathogenicity islands (SPIs) was also confirmed. Components of the type III and IV secretion systems (T3SS and T4SS) varied in different isolates, which could explain in part, differences of their pathogenicity in humans and/or persistence in broilers. Conserved clusters of genes in the T3SS were detected that could be used in designing effective strategies (diagnostic, vaccination or treatments) to combat Salmonella. Antibiotic resistance genes (CMY, aadA, ampC, florR, sul1, sulI, tetAB, and srtA) and class I integrons were detected in resistant isolates while all isolates carried multidrug efflux pump systems regardless of their antibiotic susceptibility profile.

Conclusions/significance: This study showed that the predominant Salmonella serovars in broiler chickens harbor genes encoding adhesins, flagellar proteins, T3SS, iron acquisition systems, and antibiotic and metal resistance genes that may explain their pathogenicity, colonization ability and persistence in chicken. The existence of mobile genetic elements indicates that isolates from a given serovar could acquire and transfer genetic material. Conserved genes in the T3SS and T4SS that we have identified are promising candidates for identification of diagnostic, antimicrobial or vaccine targets for the control of Salmonella in broiler chickens.

No MeSH data available.


Related in: MedlinePlus

Heatmap of 647 proteins matching to the MVirDB database.Another 784 ubiquitous proteins are not shown. Colors are consistent with Fig 2; column labels are shown in S4 Fig.
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pone.0128773.g007: Heatmap of 647 proteins matching to the MVirDB database.Another 784 ubiquitous proteins are not shown. Colors are consistent with Fig 2; column labels are shown in S4 Fig.

Mentions: We compared antibiotic and metal resistance genes of the studied Salmonella genomes to identify different mechanisms of resistance (Fig 7, S4 Fig). A total of 181 protein clusters were found to be associated with defence and resistance attributes based on matches to MVirDB. Among them, 152 clusters were found in our newly sequenced Salmonella genomes, with 101 of these present in all 25 Salmonella isolates. Several identified efflux systems are known to pump a wide range of toxic molecules including antibiotics, metals, detergents and bile salts, out of the bacterial cell. Among them the AcrABC and MdtC systems of the resistance-modulated cell division (RND) family efflux, as well as the EmrABC operon encoding the major facilitator superfamily (MFS) multidrug efflux pump were found in all 25 isolates. Two other multiple antibiotic-resistance (mar) regulons, marR (DNA-binding transcriptional repressor) and the marABC system, known to confer resistance to various antibiotics such as cephalosporins and tetracycline, were also found in all studied isolates. Apart from the isolate SALH-394-2 of serovar Typhimurium which harbored the floR gene, no chloramphenicol resistance gene cluster was found in the studied Salmonella genomes. The sulfonamide resistance gene dihydropteroate synthase type-2 (sul2) was also detected in this isolate. The Zn-dependent hydrolase β-lactamase, and the streptomycin 3''-O-adenyltransferase genes were identified in all 25 isolates while the AmpC-like beta-lactamase (blaCMY-2) was found in 13 of them (four Typhimurium, two Enteritidis, all four Heidelberg, one Hadar and two Kentucky). The transposon Tn21 resolvase TnpR and the tetracycline efflux tetA gene were found in all three isolates of serovar Hadar, however only the dihydropteroate synthase sul1 gene known to be associated with the Class 1 integron, the aminoglycoside 3-N-acetyltransferase (aac3-VI) and the aminoglycoside adenyltransferase gene (aadA) were detected in one isolate (ABBSB1020-2) of this serovar.


Genomic Comparison of Non-Typhoidal Salmonella enterica Serovars Typhimurium, Enteritidis, Heidelberg, Hadar and Kentucky Isolates from Broiler Chickens.

Dhanani AS, Block G, Dewar K, Forgetta V, Topp E, Beiko RG, Diarra MS - PLoS ONE (2015)

Heatmap of 647 proteins matching to the MVirDB database.Another 784 ubiquitous proteins are not shown. Colors are consistent with Fig 2; column labels are shown in S4 Fig.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4470630&req=5

pone.0128773.g007: Heatmap of 647 proteins matching to the MVirDB database.Another 784 ubiquitous proteins are not shown. Colors are consistent with Fig 2; column labels are shown in S4 Fig.
Mentions: We compared antibiotic and metal resistance genes of the studied Salmonella genomes to identify different mechanisms of resistance (Fig 7, S4 Fig). A total of 181 protein clusters were found to be associated with defence and resistance attributes based on matches to MVirDB. Among them, 152 clusters were found in our newly sequenced Salmonella genomes, with 101 of these present in all 25 Salmonella isolates. Several identified efflux systems are known to pump a wide range of toxic molecules including antibiotics, metals, detergents and bile salts, out of the bacterial cell. Among them the AcrABC and MdtC systems of the resistance-modulated cell division (RND) family efflux, as well as the EmrABC operon encoding the major facilitator superfamily (MFS) multidrug efflux pump were found in all 25 isolates. Two other multiple antibiotic-resistance (mar) regulons, marR (DNA-binding transcriptional repressor) and the marABC system, known to confer resistance to various antibiotics such as cephalosporins and tetracycline, were also found in all studied isolates. Apart from the isolate SALH-394-2 of serovar Typhimurium which harbored the floR gene, no chloramphenicol resistance gene cluster was found in the studied Salmonella genomes. The sulfonamide resistance gene dihydropteroate synthase type-2 (sul2) was also detected in this isolate. The Zn-dependent hydrolase β-lactamase, and the streptomycin 3''-O-adenyltransferase genes were identified in all 25 isolates while the AmpC-like beta-lactamase (blaCMY-2) was found in 13 of them (four Typhimurium, two Enteritidis, all four Heidelberg, one Hadar and two Kentucky). The transposon Tn21 resolvase TnpR and the tetracycline efflux tetA gene were found in all three isolates of serovar Hadar, however only the dihydropteroate synthase sul1 gene known to be associated with the Class 1 integron, the aminoglycoside 3-N-acetyltransferase (aac3-VI) and the aminoglycoside adenyltransferase gene (aadA) were detected in one isolate (ABBSB1020-2) of this serovar.

Bottom Line: The colonization of the chicken gut by S. enterica could result in the contamination of the environment and food chain.Genes associated with the IncF plasmid and the IncI1 plasmid were identified in twelve and four isolates, respectively, while genes associated with the IncQ plasmid were found in one isolate.The presence of numerous genes associated with Salmonella pathogenicity islands (SPIs) was also confirmed.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Computer Science, Dalhousie University, Halifax, Nova Scotia, B3H 4R2, Canada.

ABSTRACT

Background: Non-typhoidal Salmonella enterica serovars, associated with different foods including poultry products, are important causes of bacterial gastroenteritis worldwide. The colonization of the chicken gut by S. enterica could result in the contamination of the environment and food chain. The aim of this study was to compare the genomes of 25 S. enterica serovars isolated from broiler chicken farms to assess their intra- and inter-genetic variability, with a focus on virulence and antibiotic resistance characteristics.

Methodology/principal finding: The genomes of 25 S. enterica isolates covering five serovars (ten Typhimurium including three monophasic 4,[5],12:i:, four Enteritidis, three Hadar, four Heidelberg and four Kentucky) were sequenced. Most serovars were clustered in strongly supported phylogenetic clades, except for isolates of serovar Enteritidis that were scattered throughout the tree. Plasmids of varying sizes were detected in several isolates independently of serovars. Genes associated with the IncF plasmid and the IncI1 plasmid were identified in twelve and four isolates, respectively, while genes associated with the IncQ plasmid were found in one isolate. The presence of numerous genes associated with Salmonella pathogenicity islands (SPIs) was also confirmed. Components of the type III and IV secretion systems (T3SS and T4SS) varied in different isolates, which could explain in part, differences of their pathogenicity in humans and/or persistence in broilers. Conserved clusters of genes in the T3SS were detected that could be used in designing effective strategies (diagnostic, vaccination or treatments) to combat Salmonella. Antibiotic resistance genes (CMY, aadA, ampC, florR, sul1, sulI, tetAB, and srtA) and class I integrons were detected in resistant isolates while all isolates carried multidrug efflux pump systems regardless of their antibiotic susceptibility profile.

Conclusions/significance: This study showed that the predominant Salmonella serovars in broiler chickens harbor genes encoding adhesins, flagellar proteins, T3SS, iron acquisition systems, and antibiotic and metal resistance genes that may explain their pathogenicity, colonization ability and persistence in chicken. The existence of mobile genetic elements indicates that isolates from a given serovar could acquire and transfer genetic material. Conserved genes in the T3SS and T4SS that we have identified are promising candidates for identification of diagnostic, antimicrobial or vaccine targets for the control of Salmonella in broiler chickens.

No MeSH data available.


Related in: MedlinePlus