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Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts

Salmonella enterica subspecies I (ssp 1) is the leading cause of hospitalizations and deaths due to known bacterial foodborne pathogens in the United States and is frequently implicated in foodborne disease outbreaks associated with spices and nuts. However, the underlying mechanisms of this associa...

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Autores principales: Li, Ye, Salazar, Joelle K., He, Yingshu, Desai, Prerak, Porwollik, Steffen, Chu, Weiping, Paola, Palma-Salgado Sindy, Tortorello, Mary Lou, Juarez, Oscar, Feng, Hao, McClelland, Michael, Zhang, Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7644838/
https://www.ncbi.nlm.nih.gov/pubmed/33193218
http://dx.doi.org/10.3389/fmicb.2020.582202
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author Li, Ye
Salazar, Joelle K.
He, Yingshu
Desai, Prerak
Porwollik, Steffen
Chu, Weiping
Paola, Palma-Salgado Sindy
Tortorello, Mary Lou
Juarez, Oscar
Feng, Hao
McClelland, Michael
Zhang, Wei
author_facet Li, Ye
Salazar, Joelle K.
He, Yingshu
Desai, Prerak
Porwollik, Steffen
Chu, Weiping
Paola, Palma-Salgado Sindy
Tortorello, Mary Lou
Juarez, Oscar
Feng, Hao
McClelland, Michael
Zhang, Wei
author_sort Li, Ye
collection PubMed
description Salmonella enterica subspecies I (ssp 1) is the leading cause of hospitalizations and deaths due to known bacterial foodborne pathogens in the United States and is frequently implicated in foodborne disease outbreaks associated with spices and nuts. However, the underlying mechanisms of this association have not been fully elucidated. In this study, we evaluated the influence of storage temperature (4 or 25°C), relative humidity (20 or 60%), and food surface characteristics on the attachment and survival of five individual strains representing S. enterica ssp 1 serovars Typhimurium, Montevideo, Braenderup, Mbandaka, and Enteritidis on raw in-shell black peppercorns, almonds, and hazelnuts. We observed a direct correlation between the food surface roughness and S. enterica ssp 1 attachment, and detected significant inter-strain difference in survival on the shell surface under various storage conditions. A combination of low relative humidity (20%) and ambient storage temperature (25°C) resulted in the most significant reduction of S. enterica on shell surfaces (p < 0.05). To identify genes potentially associated with S. enterica attachment and survival on shell surfaces, we inoculated a library of 120,000 random transposon insertion mutants of an S. Enteritidis strain on almond shells, and screened for mutant survival after 1, 3, 7, and 14 days of storage at 20% relative humidity and 25°C. Mutants in 155 S. Enteritidis genes which are involved in carbohydrate metabolic pathways, aerobic and anaerobic respiration, inner membrane transport, and glutamine synthesis displayed significant selection on almond shells (p < 0.05). Findings of this study suggest that various food attributes, environmental factors, and an unexpectedly complex metabolic and regulatory network in S. enterica ssp 1 collectively contribute to the bacterial attachment and survival on low moisture shell surface, providing new data for the future development of knowledge-based intervention strategies.
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spelling pubmed-76448382020-11-13 Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts Li, Ye Salazar, Joelle K. He, Yingshu Desai, Prerak Porwollik, Steffen Chu, Weiping Paola, Palma-Salgado Sindy Tortorello, Mary Lou Juarez, Oscar Feng, Hao McClelland, Michael Zhang, Wei Front Microbiol Microbiology Salmonella enterica subspecies I (ssp 1) is the leading cause of hospitalizations and deaths due to known bacterial foodborne pathogens in the United States and is frequently implicated in foodborne disease outbreaks associated with spices and nuts. However, the underlying mechanisms of this association have not been fully elucidated. In this study, we evaluated the influence of storage temperature (4 or 25°C), relative humidity (20 or 60%), and food surface characteristics on the attachment and survival of five individual strains representing S. enterica ssp 1 serovars Typhimurium, Montevideo, Braenderup, Mbandaka, and Enteritidis on raw in-shell black peppercorns, almonds, and hazelnuts. We observed a direct correlation between the food surface roughness and S. enterica ssp 1 attachment, and detected significant inter-strain difference in survival on the shell surface under various storage conditions. A combination of low relative humidity (20%) and ambient storage temperature (25°C) resulted in the most significant reduction of S. enterica on shell surfaces (p < 0.05). To identify genes potentially associated with S. enterica attachment and survival on shell surfaces, we inoculated a library of 120,000 random transposon insertion mutants of an S. Enteritidis strain on almond shells, and screened for mutant survival after 1, 3, 7, and 14 days of storage at 20% relative humidity and 25°C. Mutants in 155 S. Enteritidis genes which are involved in carbohydrate metabolic pathways, aerobic and anaerobic respiration, inner membrane transport, and glutamine synthesis displayed significant selection on almond shells (p < 0.05). Findings of this study suggest that various food attributes, environmental factors, and an unexpectedly complex metabolic and regulatory network in S. enterica ssp 1 collectively contribute to the bacterial attachment and survival on low moisture shell surface, providing new data for the future development of knowledge-based intervention strategies. Frontiers Media S.A. 2020-10-23 /pmc/articles/PMC7644838/ /pubmed/33193218 http://dx.doi.org/10.3389/fmicb.2020.582202 Text en Copyright © 2020 Li, Salazar, He, Desai, Porwollik, Chu, Paola, Tortorello, Juarez, Feng, McClelland and Zhang. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Li, Ye
Salazar, Joelle K.
He, Yingshu
Desai, Prerak
Porwollik, Steffen
Chu, Weiping
Paola, Palma-Salgado Sindy
Tortorello, Mary Lou
Juarez, Oscar
Feng, Hao
McClelland, Michael
Zhang, Wei
Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts
title Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts
title_full Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts
title_fullStr Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts
title_full_unstemmed Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts
title_short Mechanisms of Salmonella Attachment and Survival on In-Shell Black Peppercorns, Almonds, and Hazelnuts
title_sort mechanisms of salmonella attachment and survival on in-shell black peppercorns, almonds, and hazelnuts
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7644838/
https://www.ncbi.nlm.nih.gov/pubmed/33193218
http://dx.doi.org/10.3389/fmicb.2020.582202
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