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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Autores principales:	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
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	Salmonella multidrug resistance (MDR) plasmid Salmonella genomic island (SGI) Salmonella pathogenicity island (SPI) Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/983a5b831eab436e926cf47ce752851f
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spelling	oai:doaj.org-article:983a5b831eab436e926cf47ce752851f2021-11-19T06:57:02ZLong-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica1664-302X10.3389/fmicb.2021.777817https://doaj.org/article/983a5b831eab436e926cf47ce752851f2021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fmicb.2021.777817/fullhttps://doaj.org/toc/1664-302XSalmonella 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.Cong LiGregory H. TysonChih-Hao HsuLucas HarrisonErrol StrainThu-Thuy TranGlenn E. TillmanUday DessaiPatrick F. McDermottShaohua ZhaoFrontiers Media S.A.articleSalmonellamultidrug resistance (MDR)plasmidSalmonella genomic island (SGI)Salmonella pathogenicity island (SPI)MicrobiologyQR1-502ENFrontiers in Microbiology, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Salmonella multidrug resistance (MDR) plasmid Salmonella genomic island (SGI) Salmonella pathogenicity island (SPI) Microbiology QR1-502
spellingShingle	Salmonella multidrug resistance (MDR) plasmid Salmonella genomic island (SGI) Salmonella pathogenicity island (SPI) Microbiology QR1-502 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
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.
format	article
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
title	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_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_sort	long-read sequencing reveals evolution and acquisition of antimicrobial resistance and virulence genes in salmonella enterica
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/983a5b831eab436e926cf47ce752851f
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Long-Read Sequencing Reveals Evolution and Acquisition of Antimicrobial Resistance and Virulence Genes in Salmonella enterica

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