Sub-lethal stress-induced cross-protection against ultraviolet-C in Salmonella enterica on raw whole almonds and fresh-cut leafy greens
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 <i>Salmonella enterica</i> to ultraviolet-C (UV-C) treatments on raw whole almonds (RWAs) and fresh-cut leafy greens (FCLGs), investigated the role of <i>rpoS</i> in stress-induced cross-protection, and evaluated <i>Enterococcus faecium</i> NRRL B-2354 as a surrogate for <i>S. enterica</i>. 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 <i>S. enterica</i> strains, along with <i>S.</i> Typhimurium ATCC 14028 and its Δ<i>rpoS</i> mutant (IB43), were exposed to desiccation stress, heat shock, oxidation stress, or acid stress. Afterward, stressed and unstressed cells were inoculated onto RWAs and FCLGs, and treated with UV-C (500 μW/cm<sup>2</sup>, 60 min). Treated FCLGs were then stored under cold or temperature abuse condition for 7 days. Results showed that acid-stressed <i>S. enterica</i> exhibited greater UV-C resistance on RWAs, while oxidation-stressed cells had increased survival on FCLGs (<i>p</i> < 0.05). Under temperature abuse, unstressed, oxidation-stressed, or acid-stressed <i>S. enterica</i> were inactivated faster, whereas heat-shocked cells persisted until Day 7. Desiccation-stressed cells rebounded temporarily before inactivation by Day 7. IB43 was more susceptible to UV-C (<i>p</i> < 0.05) than the wild-type strain and lacked cross-protection from prior sub-lethal stress exposure, confirming the crucial role of <i>rpoS</i> in UV-C resistance and stress adaptation. NRRL B-2354 demonstrated comparable or greater survival than <i>S. enterica</i>, supporting its use as a suitable surrogate. These findings highlight the influence of sub-lethal stress on UV-C resistance in <i>S. enterica</i> and emphasize the importance of including stress-adapted pathogens in challenge studies to improve food safety.
Authors
- Shirley Ann Micallef (ORCID: https://orcid.org/0000-0003-0041-2139)
- Zhao Chen (ORCID: https://orcid.org/0000-0002-1784-167X)
- Jie Zheng (ORCID: https://orcid.org/0000-0003-3447-9681)
- Jianghong Meng (ORCID: https://orcid.org/0000-0002-8623-6764)
Institutions
- Center for Food Safety and Applied Nutrition (US)
- United States Food and Drug Administration (US)
- Food and Drug Administration (TH)
- University of Maryland, College Park (US)
Publication Details
- Journal
- Frontiers in Microbiology
- Published
- 2025-06-18
- DOI
- https://doi.org/10.3389/fmicb.2025.1599380
- Citations
- 3
- Primary Topic
- Listeria monocytogenes in Food Safety
- Type
- article
- Field-Weighted Citation Impact
- 3.70
Funders
- U.S. Department of Agriculture
- University of Washington
- National Institute of Food and Agriculture