Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride

ABSTRACTSalmonella enterica is a prominent cause of foodborne disease in the United States. However, the mechanism and route of pathogen transmission that leads to Salmonella infection in commercial processing plants are poorly understood. This study aimed to investigate the effect of mixed-species...

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Main Authors: Qiyue Chen, Vignesh Palanisamy, Rong Wang, Joseph M. Bosilevac, Sapna Chitlapilly Dass
Format: Article
Language:English
Published: American Society for Microbiology 2024-02-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02346-23
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author Qiyue Chen
Vignesh Palanisamy
Rong Wang
Joseph M. Bosilevac
Sapna Chitlapilly Dass
author_facet Qiyue Chen
Vignesh Palanisamy
Rong Wang
Joseph M. Bosilevac
Sapna Chitlapilly Dass
author_sort Qiyue Chen
collection DOAJ
description ABSTRACTSalmonella enterica is a prominent cause of foodborne disease in the United States. However, the mechanism and route of pathogen transmission that leads to Salmonella infection in commercial processing plants are poorly understood. This study aimed to investigate the effect of mixed-species biofilms on S. enterica survival and persistence under sanitizer stress [Quaternary ammonium compounds (QACs)] by analyzing 78 floor drain samples from a meat processing facility and three S. enterica strains (serovars Cerro, Montevideo, and Typhimurium) isolated from that facility and an unrelated source. The four test groups were as follows: control, QAC treatment, Salmonella addition, and QAC treatment with Salmonella addition. DNAs were extracted, and 16S rRNA gene based on the variable region V4 amplicon sequencing was performed to analyze the relative abundance, core microbiome, and Alpha and Beta diversity using the qiime2 pipeline. At the genus level, the Brochothrix (45.56%), Pseudomonas (38.94%), Carnobacterium (6.18%), Lactococcus (4.68%), Serratia (3.14%), and Staphylococcus (0.82%) were shown to be the most prevalent in all drain samples. The results demonstrate that the relative abundance of different bacterial genera was affected by both QAC treatment and Salmonella addition, with some genera showing increases or decreases in abundance. Notably, the correlation network was constructed to understand the relationships between the different bacteria. Nitrospira had the greatest number of connections in the floor drain environment network, with two negative and eight positive correlations. The results suggest that Nitrospira in the mixed-species biofilm community may play a role in converting ammonium in the QAC sanitizer into nitrites. Thus, Nitrospira could be a potentially important genus in providing sanitizer resistance to pathogen-encompassed mixed-species biofilms.IMPORTANCESalmonella contamination in meat processing facilities can lead to foodborne illness outbreaks. Our study characterized the microbiome dynamics in beef facility drains and their response to Salmonella addition and common sanitizer (QAC). Nitrospira could be an important genus in providing sanitizer resistance to pathogen-encompassed mixed-species biofilms. The results provide insight into the impact of mixed-species biofilms on Salmonella survival and persistence under sanitizer stress in meat processing facilities. The results highlight the need to consider mixed-species biofilm effects when developing targeted interventions to enhance food safety.
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spelling doaj.art-fea99f6e15cc451596d458ab2b9ff4812024-02-06T14:04:55ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-02-0112210.1128/spectrum.02346-23Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chlorideQiyue Chen0Vignesh Palanisamy1Rong Wang2Joseph M. Bosilevac3Sapna Chitlapilly Dass4Department of Animal Science, Texas A&M University, College Station, Texas, USADepartment of Animal Science, Texas A&M University, College Station, Texas, USAU. S. Department of Agriculture, Roman L. Hruska U.S. Meat Animal Research Center, Lincoln, Nebraska, USAU. S. Department of Agriculture, Roman L. Hruska U.S. Meat Animal Research Center, Lincoln, Nebraska, USADepartment of Animal Science, Texas A&M University, College Station, Texas, USAABSTRACTSalmonella enterica is a prominent cause of foodborne disease in the United States. However, the mechanism and route of pathogen transmission that leads to Salmonella infection in commercial processing plants are poorly understood. This study aimed to investigate the effect of mixed-species biofilms on S. enterica survival and persistence under sanitizer stress [Quaternary ammonium compounds (QACs)] by analyzing 78 floor drain samples from a meat processing facility and three S. enterica strains (serovars Cerro, Montevideo, and Typhimurium) isolated from that facility and an unrelated source. The four test groups were as follows: control, QAC treatment, Salmonella addition, and QAC treatment with Salmonella addition. DNAs were extracted, and 16S rRNA gene based on the variable region V4 amplicon sequencing was performed to analyze the relative abundance, core microbiome, and Alpha and Beta diversity using the qiime2 pipeline. At the genus level, the Brochothrix (45.56%), Pseudomonas (38.94%), Carnobacterium (6.18%), Lactococcus (4.68%), Serratia (3.14%), and Staphylococcus (0.82%) were shown to be the most prevalent in all drain samples. The results demonstrate that the relative abundance of different bacterial genera was affected by both QAC treatment and Salmonella addition, with some genera showing increases or decreases in abundance. Notably, the correlation network was constructed to understand the relationships between the different bacteria. Nitrospira had the greatest number of connections in the floor drain environment network, with two negative and eight positive correlations. The results suggest that Nitrospira in the mixed-species biofilm community may play a role in converting ammonium in the QAC sanitizer into nitrites. Thus, Nitrospira could be a potentially important genus in providing sanitizer resistance to pathogen-encompassed mixed-species biofilms.IMPORTANCESalmonella contamination in meat processing facilities can lead to foodborne illness outbreaks. Our study characterized the microbiome dynamics in beef facility drains and their response to Salmonella addition and common sanitizer (QAC). Nitrospira could be an important genus in providing sanitizer resistance to pathogen-encompassed mixed-species biofilms. The results provide insight into the impact of mixed-species biofilms on Salmonella survival and persistence under sanitizer stress in meat processing facilities. The results highlight the need to consider mixed-species biofilm effects when developing targeted interventions to enhance food safety.https://journals.asm.org/doi/10.1128/spectrum.02346-23biofilmSalmonellasanitizerQAC
spellingShingle Qiyue Chen
Vignesh Palanisamy
Rong Wang
Joseph M. Bosilevac
Sapna Chitlapilly Dass
Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride
Microbiology Spectrum
biofilm
Salmonella
sanitizer
QAC
title Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride
title_full Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride
title_fullStr Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride
title_full_unstemmed Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride
title_short Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride
title_sort salmonella induced microbiome profile in response to sanitation by quaternary ammonium chloride
topic biofilm
Salmonella
sanitizer
QAC
url https://journals.asm.org/doi/10.1128/spectrum.02346-23
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AT rongwang salmonellainducedmicrobiomeprofileinresponsetosanitationbyquaternaryammoniumchloride
AT josephmbosilevac salmonellainducedmicrobiomeprofileinresponsetosanitationbyquaternaryammoniumchloride
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