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.

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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

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article

Sub-lethal stress-induced cross-protection against ultraviolet-C in Salmonella enterica on raw whole almonds and fresh-cut leafy greens

Shirley Ann Micallef, Zhao Chen, Jie Zheng, Jianghong Meng
3 citations
Frontiers in Microbiology
Listeria monocytogenes in Food Safety
3.70
article

Sub-lethal stress-induced cross-protection against ultraviolet-C in Salmonella enterica on raw whole almonds and fresh-cut leafy greens

Shirley Ann Micallef, Zhao Chen, Jie Zheng, Jianghong Meng
article en
3 citations

Abstract

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.

Frontiers in MicrobiologyVol. 16
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)
U.S. Department of Agriculture, University of Washington, National Institute of Food and Agriculture
Openalex Percentile: Top 8%
Listeria monocytogenes in Food Safety
3.70
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