Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica
Salmonella enterica is a significant and phylogenetically diverse zoonotic pathogen. To understand its genomic heterogeneity and antimicrobial resistance, we performed long-read sequencing on Salmonella isolated from retail meats and food animals. A collection of 134 multidrug-resistant isolates bel...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-11-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.777817/full |
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| author | Cong Li Gregory H. Tyson Chih-Hao Hsu Lucas Harrison Errol Strain Thu-Thuy Tran Glenn E. Tillman Uday Dessai Patrick F. McDermott Shaohua Zhao |
| author_facet | Cong Li Gregory H. Tyson Chih-Hao Hsu Lucas Harrison Errol Strain Thu-Thuy Tran Glenn E. Tillman Uday Dessai Patrick F. McDermott Shaohua Zhao |
| author_sort | Cong Li |
| collection | DOAJ |
| description | Salmonella enterica is a significant and phylogenetically diverse zoonotic pathogen. To understand its genomic heterogeneity and antimicrobial resistance, we performed long-read sequencing on Salmonella isolated from retail meats and food animals. A collection of 134 multidrug-resistant isolates belonging to 33 serotypes were subjected to PacBio sequencing. One major locus of diversity among these isolates was the presence and orientation of Salmonella pathogenic islands (SPI), which varied across different serotypes but were largely conserved within individual serotypes. We also identified insertion of an IncQ resistance plasmid into the chromosome of fourteen strains of serotype I 4,[5],12:i:– and the Salmonella genomic island 1 (SGI-1) in five serotypes. The presence of various SPIs, SGI-1 and integrated plasmids contributed significantly to the genomic variability and resulted in chromosomal resistance in 55.2% (74/134) of the study isolates. A total of 93.3% (125/134) of isolates carried at least one plasmid, with isolates carrying up to seven plasmids. We closed 233 plasmid sequences of thirteen replicon types, along with twelve hybrid plasmids. Some associations between Salmonella isolate source, serotype, and plasmid type were seen. For instance, IncX plasmids were more common in serotype Kentucky from retail chicken. Plasmids IncC and IncHI had on average more than five antimicrobial resistance genes, whereas in IncX, it was less than one per plasmid. Overall, 60% of multidrug resistance (MDR) strains that carried >3 AMR genes also carried >3 heavy metal resistance genes, raising the possibility of co-selection of antimicrobial resistance in the presence of heavy metals. We also found nine isolates representing four serotypes that carried virulence plasmids with the spv operon. Together, these data demonstrate the power of long-read sequencing to reveal genomic arrangements and integrated plasmids with a high level of resolution for tracking and comparing resistant strains from different sources. Additionally, the findings from this study will help expand the reference set of closed Salmonella genomes that can be used to improve genome assembly from short-read data commonly used in One Health antimicrobial resistance surveillance. |
| first_indexed | 2024-12-13T16:43:24Z |
| format | Article |
| id | doaj.art-983a5b831eab436e926cf47ce752851f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-13T16:43:24Z |
| publishDate | 2021-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-983a5b831eab436e926cf47ce752851f2022-12-21T23:38:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-11-011210.3389/fmicb.2021.777817777817Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella entericaCong Li0Gregory H. Tyson1Chih-Hao Hsu2Lucas Harrison3Errol Strain4Thu-Thuy Tran5Glenn E. Tillman6Uday Dessai7Patrick F. McDermott8Shaohua Zhao9Center for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesCenter for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesCenter for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesCenter for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesCenter for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesCenter for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesFood Safety and Inspection Service, United States Department of Agriculture, Athens, GA, United StatesFood Safety and Inspection Service, United States Department of Agriculture, Washington, DC, United StatesCenter for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesCenter for Veterinary Medicine, United States Food and Drug Administration, Laurel, MD, United StatesSalmonella enterica is a significant and phylogenetically diverse zoonotic pathogen. To understand its genomic heterogeneity and antimicrobial resistance, we performed long-read sequencing on Salmonella isolated from retail meats and food animals. A collection of 134 multidrug-resistant isolates belonging to 33 serotypes were subjected to PacBio sequencing. One major locus of diversity among these isolates was the presence and orientation of Salmonella pathogenic islands (SPI), which varied across different serotypes but were largely conserved within individual serotypes. We also identified insertion of an IncQ resistance plasmid into the chromosome of fourteen strains of serotype I 4,[5],12:i:– and the Salmonella genomic island 1 (SGI-1) in five serotypes. The presence of various SPIs, SGI-1 and integrated plasmids contributed significantly to the genomic variability and resulted in chromosomal resistance in 55.2% (74/134) of the study isolates. A total of 93.3% (125/134) of isolates carried at least one plasmid, with isolates carrying up to seven plasmids. We closed 233 plasmid sequences of thirteen replicon types, along with twelve hybrid plasmids. Some associations between Salmonella isolate source, serotype, and plasmid type were seen. For instance, IncX plasmids were more common in serotype Kentucky from retail chicken. Plasmids IncC and IncHI had on average more than five antimicrobial resistance genes, whereas in IncX, it was less than one per plasmid. Overall, 60% of multidrug resistance (MDR) strains that carried >3 AMR genes also carried >3 heavy metal resistance genes, raising the possibility of co-selection of antimicrobial resistance in the presence of heavy metals. We also found nine isolates representing four serotypes that carried virulence plasmids with the spv operon. Together, these data demonstrate the power of long-read sequencing to reveal genomic arrangements and integrated plasmids with a high level of resolution for tracking and comparing resistant strains from different sources. Additionally, the findings from this study will help expand the reference set of closed Salmonella genomes that can be used to improve genome assembly from short-read data commonly used in One Health antimicrobial resistance surveillance.https://www.frontiersin.org/articles/10.3389/fmicb.2021.777817/fullSalmonellamultidrug resistance (MDR)plasmidSalmonella genomic island (SGI)Salmonella pathogenicity island (SPI) |
| spellingShingle | Cong Li Gregory H. Tyson Chih-Hao Hsu Lucas Harrison Errol Strain Thu-Thuy Tran Glenn E. Tillman Uday Dessai Patrick F. McDermott Shaohua Zhao Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica Frontiers in Microbiology Salmonella multidrug resistance (MDR) plasmid Salmonella genomic island (SGI) Salmonella pathogenicity island (SPI) |
| title | Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica |
| title_full | Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica |
| title_fullStr | Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica |
| title_full_unstemmed | Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica |
| title_short | Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica |
| title_sort | long read sequencing reveals evolution and acquisition of antimicrobial resistance and virulence genes in salmonella enterica |
| topic | Salmonella multidrug resistance (MDR) plasmid Salmonella genomic island (SGI) Salmonella pathogenicity island (SPI) |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.777817/full |
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