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

Authors: CHEN, QIYUE - Texas A&M University; PALANISAMY, VIGNESH - Texas A&M University; Wang, Rong; Bosilevac, Joseph - Mick; CHITAPILLY DASS, SAPNA - Texas A&M University

Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/21/2023
Publication Date: 1/16/2024
Citation: Chen, Q., Palanisamy, V., Wang, R., Bosilevac, J.M., Chitapilly Dass, S. 2024. Salmonella-induced microbiome profile in response to sanitation by quaternary ammonium chloride. Microbiology Spectrum. 12(2). Article 02346-23. https://doi.org/10.1128/spectrum.02346-23.
DOI: https://doi.org/10.1128/spectrum.02346-23

Interpretive Summary: In the United States, Salmonella enterica is a leading cause of bacterial foodborne illnesses which is related to the consumption of contaminated foods including beef products. One potential Salmonella contamination route at meat plants could be that certain Salmonella strains are better adapted to the processing environment through mixed biofilm formation, meaning Salmonella cell aggregates colonized with other environmental bacteria on contact surface so that they can better tolerate and survive the sanitization procedures and may subsequently cause product contamination. This study used floor drain samples as representatives of environmental bacteria to investigate the impact of Salmonella biofilm formation with the environmental bacteria on Salmonella survival and persistence in a beef plant. Results showed there were six major bacterial species present in the plant environment. Salmonella colonization and treatment with a common sanitizer quaternary ammonium chloride (QAC) changed the percentages of the various bacteria in the environment. An environmental bacterial species Nitrospira that can convert QAC residues to nitrites had the most interactions with other bacteria in the QAC-treated community, suggesting this species might play a critical role in conferring chemical tolerance to the mixed biofilms containing multiple species of bacteria including Salmonella. The study provides insight into the impact of environmental mixed biofilms on Salmonella survival and persistence under sanitizer stress in meat processing facilities.

Technical Abstract: Salmonella 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. IMPORTANCE-Salmonella 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.