Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America

ABSTRACT Two separate human outbreaks of Salmonella enterica serotype Reading occurred between 2017 and 2019 in the United States and Canada, and both outbreaks were linked to the consumption of raw turkey products. In this study, a comprehensive genomic investigation was conducted to reconstruct th...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Elizabeth A. Miller, Ehud Elnekave, Cristian Flores-Figueroa, Abigail Johnson, Ashley Kearney, Jeannette Munoz-Aguayo, Kaitlin A. Tagg, Lorelee Tschetter, Bonnie P. Weber, Celine A. Nadon, Dave Boxrud, Randall S. Singer, Jason P. Folster, Timothy J. Johnson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Salmonella clone genomic human outbreak poultry Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5c87c6389c2640238605f63c6c2e4a6c
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:5c87c6389c2640238605f63c6c2e4a6c
record_format	dspace
spelling	oai:doaj.org-article:5c87c6389c2640238605f63c6c2e4a6c2021-11-15T15:29:16ZEmergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America10.1128/mSphere.00056-202379-5042https://doaj.org/article/5c87c6389c2640238605f63c6c2e4a6c2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00056-20https://doaj.org/toc/2379-5042ABSTRACT Two separate human outbreaks of Salmonella enterica serotype Reading occurred between 2017 and 2019 in the United States and Canada, and both outbreaks were linked to the consumption of raw turkey products. In this study, a comprehensive genomic investigation was conducted to reconstruct the evolutionary history of S. Reading from turkeys and to determine the genomic context of outbreaks involving this infrequently isolated Salmonella serotype. A total of 988 isolates of U.S. origin were examined using whole-genome-based approaches, including current and historical isolates from humans, meat, and live food animals. Broadly, isolates clustered into three major clades, with one apparently highly adapted turkey clade. Within the turkey clade, isolates clustered into three subclades, including an “emergent” clade that contained only isolates dated 2016 or later, with many of the isolates from these outbreaks. Genomic differences were identified between emergent and other turkey subclades, suggesting that the apparent success of currently circulating subclades is, in part, attributable to plasmid acquisitions conferring antimicrobial resistance, gain of phage-like sequences with cargo virulence factors, and mutations in systems that may be involved in beta-glucuronidase activity and resistance towards colicins. U.S. and Canadian outbreak isolates were found interspersed throughout the emergent subclade and the other circulating subclade. The emergence of a novel S. Reading turkey subclade, coinciding temporally with expansion in commercial turkey production and with U.S. and Canadian human outbreaks, indicates that emergent strains with higher potential for niche success were likely vertically transferred and rapidly disseminated from a common source. IMPORTANCE Increasingly, outbreak investigations involving foodborne pathogens are difficult due to the interconnectedness of food animal production and distribution, and homogeneous nature of industry integration, necessitating high-resolution genomic investigations to determine their basis. Fortunately, surveillance and whole-genome sequencing, combined with the public availability of these data, enable comprehensive queries to determine underlying causes of such outbreaks. Utilizing this pipeline, it was determined that a novel clone of Salmonella Reading has emerged that coincided with increased abundance in raw turkey products and two outbreaks of human illness in North America. The rapid dissemination of this highly adapted and conserved clone indicates that it was likely obtained from a common source and rapidly disseminated across turkey production. Key genomic changes may have contributed to its apparent continued success in commercial turkeys and ability to cause illness in humans.Elizabeth A. MillerEhud ElnekaveCristian Flores-FigueroaAbigail JohnsonAshley KearneyJeannette Munoz-AguayoKaitlin A. TaggLorelee TschetterBonnie P. WeberCeline A. NadonDave BoxrudRandall S. SingerJason P. FolsterTimothy J. JohnsonAmerican Society for MicrobiologyarticleSalmonellaclonegenomichumanoutbreakpoultryMicrobiologyQR1-502ENmSphere, Vol 5, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Salmonella clone genomic human outbreak poultry Microbiology QR1-502
spellingShingle	Salmonella clone genomic human outbreak poultry Microbiology QR1-502 Elizabeth A. Miller Ehud Elnekave Cristian Flores-Figueroa Abigail Johnson Ashley Kearney Jeannette Munoz-Aguayo Kaitlin A. Tagg Lorelee Tschetter Bonnie P. Weber Celine A. Nadon Dave Boxrud Randall S. Singer Jason P. Folster Timothy J. Johnson Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America
description	ABSTRACT Two separate human outbreaks of Salmonella enterica serotype Reading occurred between 2017 and 2019 in the United States and Canada, and both outbreaks were linked to the consumption of raw turkey products. In this study, a comprehensive genomic investigation was conducted to reconstruct the evolutionary history of S. Reading from turkeys and to determine the genomic context of outbreaks involving this infrequently isolated Salmonella serotype. A total of 988 isolates of U.S. origin were examined using whole-genome-based approaches, including current and historical isolates from humans, meat, and live food animals. Broadly, isolates clustered into three major clades, with one apparently highly adapted turkey clade. Within the turkey clade, isolates clustered into three subclades, including an “emergent” clade that contained only isolates dated 2016 or later, with many of the isolates from these outbreaks. Genomic differences were identified between emergent and other turkey subclades, suggesting that the apparent success of currently circulating subclades is, in part, attributable to plasmid acquisitions conferring antimicrobial resistance, gain of phage-like sequences with cargo virulence factors, and mutations in systems that may be involved in beta-glucuronidase activity and resistance towards colicins. U.S. and Canadian outbreak isolates were found interspersed throughout the emergent subclade and the other circulating subclade. The emergence of a novel S. Reading turkey subclade, coinciding temporally with expansion in commercial turkey production and with U.S. and Canadian human outbreaks, indicates that emergent strains with higher potential for niche success were likely vertically transferred and rapidly disseminated from a common source. IMPORTANCE Increasingly, outbreak investigations involving foodborne pathogens are difficult due to the interconnectedness of food animal production and distribution, and homogeneous nature of industry integration, necessitating high-resolution genomic investigations to determine their basis. Fortunately, surveillance and whole-genome sequencing, combined with the public availability of these data, enable comprehensive queries to determine underlying causes of such outbreaks. Utilizing this pipeline, it was determined that a novel clone of Salmonella Reading has emerged that coincided with increased abundance in raw turkey products and two outbreaks of human illness in North America. The rapid dissemination of this highly adapted and conserved clone indicates that it was likely obtained from a common source and rapidly disseminated across turkey production. Key genomic changes may have contributed to its apparent continued success in commercial turkeys and ability to cause illness in humans.
format	article
author	Elizabeth A. Miller Ehud Elnekave Cristian Flores-Figueroa Abigail Johnson Ashley Kearney Jeannette Munoz-Aguayo Kaitlin A. Tagg Lorelee Tschetter Bonnie P. Weber Celine A. Nadon Dave Boxrud Randall S. Singer Jason P. Folster Timothy J. Johnson
author_facet	Elizabeth A. Miller Ehud Elnekave Cristian Flores-Figueroa Abigail Johnson Ashley Kearney Jeannette Munoz-Aguayo Kaitlin A. Tagg Lorelee Tschetter Bonnie P. Weber Celine A. Nadon Dave Boxrud Randall S. Singer Jason P. Folster Timothy J. Johnson
author_sort	Elizabeth A. Miller
title	Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America
title_short	Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America
title_full	Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America
title_fullStr	Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America
title_full_unstemmed	Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America
title_sort	emergence of a novel <named-content content-type="genus-species">salmonella enterica</named-content> serotype reading clonal group is linked to its expansion in commercial turkey production, resulting in unanticipated human illness in north america
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/5c87c6389c2640238605f63c6c2e4a6c
work_keys_str_mv	AT elizabethamiller emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT ehudelnekave emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT cristianfloresfigueroa emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT abigailjohnson emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT ashleykearney emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT jeannettemunozaguayo emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT kaitlinatagg emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT loreleetschetter emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT bonniepweber emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT celineanadon emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT daveboxrud emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT randallssinger emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT jasonpfolster emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica AT timothyjjohnson emergenceofanovelnamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentserotypereadingclonalgroupislinkedtoitsexpansionincommercialturkeyproductionresultinginunanticipatedhumanillnessinnorthamerica
_version_	1718427887387803648

Emergence of a Novel <named-content content-type="genus-species">Salmonella enterica</named-content> Serotype Reading Clonal Group Is Linked to Its Expansion in Commercial Turkey Production, Resulting in Unanticipated Human Illness in North America

Ejemplares similares