ORIGINAL RESEARCH article
Front. Microbiol.
Sec. Food Microbiology
Volume 16 - 2025 | doi: 10.3389/fmicb.2025.1599380
This article is part of the Research TopicBacterial Persister Cells in the Food IndustryView all 6 articles
Sub-Lethal Stress-Induced Cross-Protection Against Ultraviolet-C in Salmonella enterica on Raw Whole Almonds and Fresh-Cut Leafy Greens
Provisionally accepted
- 1University of Maryland, College Park, College Park, Maryland, United States
- 2United States Food and Drug Administration, Silver Spring, Maryland, United States
Select one of your emails
You have multiple emails registered with Frontiers:
Notify me on publication
Please enter your email address:
If you already have an account, please login
You don't have a Frontiers account ? You can register here
Pre-exposure to sub-lethal stress can increase the resistance of foodborne pathogens to inactivation processes, posing potential risks to food safety. This study examined how sub-lethal stress influences the resistance of Salmonella enterica to ultraviolet-C (UV-C) treatments on raw whole almonds (RWAs) and fresh-cut leafy greens (FCLGs), investigated the role of rpoS in stress-induced crossprotection, and evaluated Enterococcus faecium NRRL B-2354 as a surrogate for S. enterica. Additionally, we assessed the survival of sub-lethally stressed cells on FCLGs under cold or temperature abuse condition post-UV-C treatment. A cocktail of three S. enterica strains, along with S. Typhimurium ATCC 14028 and its ΔrpoS mutant (IB43), were exposed to desiccation, heat shock, oxidation, or acid stress. Afterward, stressed and unstressed cells were inoculated onto RWAs and FCLGs, and treated with UV-C (500 µW/cm 2 , 60 min). Treated FCLGs were then stored under cold or temperature abuse condition for seven days. Results showed that acid-stressed S. enterica exhibited greater UV-C resistance on RWAs, while oxidation-stressed cells had increased survival on FCLGs (P < 0.05). Under temperature abuse, unstressed, oxidation-stressed, or acid-stressed S. enterica were inactivated faster, whereas heat-shocked cells persisted until Day 7. Desiccationstressed cells rebounded temporarily before inactivation by Day 7. IB43 was more susceptible to UV-C (P < 0.05) than the wild-type strain and lacked cross-protection from prior sub-lethal stress exposure, confirming the crucial role of rpoS in UV-C resistance and stress adaptation. NRRL B-2354 demonstrated comparable or greater survival than S. enterica, supporting its use as a suitable surrogate. These findings highlight the influence of sub-lethal stress on UV-C resistance in S. enterica and emphasize the importance of including stress-adapted pathogens in challenge studies to improve food safety.
Keywords: Salmonella enterica, Ultraviolet-C, almond, Leafy green, Sub-lethal stress, Crossprotection, rpoS, surrogate
Received: 24 Mar 2025; Accepted: 19 May 2025.
Copyright: © 2025 Chen, Zheng, Micallef and Meng. 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) or licensor 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.
* Correspondence:
Zhao Chen, University of Maryland, College Park, College Park, 20742, Maryland, United States
Jie Zheng, United States Food and Drug Administration, Silver Spring, 20993, Maryland, United States
Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.