{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T14:52:45Z","timestamp":1781880765248,"version":"3.54.5"},"reference-count":49,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2025,4,22]],"date-time":"2025-04-22T00:00:00Z","timestamp":1745280000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Major Projects of the Department of Education of Anhui Province","award":["2023AH040277"],"award-info":[{"award-number":["2023AH040277"]}]},{"name":"Major Projects of the Department of Education of Anhui Province","award":["2024AH010007"],"award-info":[{"award-number":["2024AH010007"]}]},{"name":"Major Projects of the Department of Education of Anhui Province","award":["2023KJCXTD003"],"award-info":[{"award-number":["2023KJCXTD003"]}]},{"name":"Excellent Research and Innovation Team of Anhui Province Universities","award":["2023AH040277"],"award-info":[{"award-number":["2023AH040277"]}]},{"name":"Excellent Research and Innovation Team of Anhui Province Universities","award":["2024AH010007"],"award-info":[{"award-number":["2024AH010007"]}]},{"name":"Excellent Research and Innovation Team of Anhui Province Universities","award":["2023KJCXTD003"],"award-info":[{"award-number":["2023KJCXTD003"]}]},{"name":"Project of the Science and Technology Innovation Team of Anhui Science and Technology University","award":["2023AH040277"],"award-info":[{"award-number":["2023AH040277"]}]},{"name":"Project of the Science and Technology Innovation Team of Anhui Science and Technology University","award":["2024AH010007"],"award-info":[{"award-number":["2024AH010007"]}]},{"name":"Project of the Science and Technology Innovation Team of Anhui Science and Technology University","award":["2023KJCXTD003"],"award-info":[{"award-number":["2023KJCXTD003"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Foods"],"abstract":"<jats:p>The traditional marination process enhances food flavor and inhibits microbial growth. However, in hyperosmotic environments, microorganisms can activate stress responses to ensure survival, potentially compromising food safety. This study investigated the osmotolerance mechanisms of Salmonella Derby (S. Derby) by comparing a wild-type strain (S. D-WT) and an osmotolerant strain (S. D-OT) under NaCl-induced hyperosmotic stress. Both strains were subjected to 0.85%, 4%, and 16% NaCl for 0, 8, and 16 days, and their growth behavior, membrane integrity, intracellular osmoprotectant content, and transcription of related genes were evaluated. By day 16, both strains showed a growth delay of approximately 3 h. S. D-OT maintained better membrane integrity and exhibited higher intracellular levels of osmoprotectants (K\u207a, trehalose, and proline), which aligned with the upregulation of the transcriptional levels of kdpC, kuP, rpoS, and proU. These findings indicated that S. D-OT achieved improved osmotic stress tolerance by regulating osmoprotectant synthesis and maintaining intracellular homeostasis. In contrast, S. D-WT displayed greater resistance to multiple antibiotics (gentamicin, ciprofloxacin, trimethoprim-sulfamethoxazole, and chloramphenicol) under 4% and 16% NaCl conditions, which may pose a higher food safety risk. Overall, this study provides insights for improving microbial control strategies in preserved foods and mitigating foodborne disease risks.<\/jats:p>","DOI":"10.3390\/foods14091440","type":"journal-article","created":{"date-parts":[[2025,4,21]],"date-time":"2025-04-21T22:35:33Z","timestamp":1745274933000},"page":"1440","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Unveiling Salmonella Derby Survival: Stress Responses to Prolonged Hyperosmotic Stress"],"prefix":"10.3390","volume":"14","author":[{"given":"Yingting","family":"Gong","sequence":"first","affiliation":[{"name":"Food Science and Engineering, Anhui Science and Technology University, Chuzhou 233100, China"},{"name":"Province Key Laboratory of Functional Agriculture and Functional Food, Anhui Science and Technology University, Chuzhou 239000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaoxuan","family":"Li","sequence":"additional","affiliation":[{"name":"Food Science and Engineering, Anhui Science and Technology University, Chuzhou 233100, China"},{"name":"Province Key Laboratory of Functional Agriculture and Functional Food, Anhui Science and Technology University, Chuzhou 239000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junying","family":"Wang","sequence":"additional","affiliation":[{"name":"Food Science and Engineering, Anhui Science and Technology University, Chuzhou 233100, China"},{"name":"Province Key Laboratory of Functional Agriculture and Functional Food, Anhui Science and Technology University, Chuzhou 239000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanyan","family":"Zhao","sequence":"additional","affiliation":[{"name":"Food Science and Engineering, Anhui Science and Technology University, Chuzhou 233100, China"},{"name":"Province Key Laboratory of Functional Agriculture and Functional Food, Anhui Science and Technology University, Chuzhou 239000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingnan","family":"Meng","sequence":"additional","affiliation":[{"name":"Food Science and Engineering, Anhui Science and Technology University, Chuzhou 233100, China"},{"name":"Province Key Laboratory of Functional Agriculture and Functional Food, Anhui Science and Technology University, Chuzhou 239000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ligong","family":"Zhai","sequence":"additional","affiliation":[{"name":"Food Science and Engineering, Anhui Science and Technology University, Chuzhou 233100, China"},{"name":"Province Key Laboratory of Functional Agriculture and Functional Food, Anhui Science and Technology University, Chuzhou 239000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,4,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"European Food Safety Authority (EFSA), and European Centre for Disease Prevention and Control (ECDC) (2024). The European Union One Health 2023 Zoonoses Report. EFSA J., 22, e9106.","DOI":"10.2903\/j.efsa.2024.9106"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Ehuwa, O., Jaiswal, A.K., and Jaiswal, S. (2021). Salmonella, Food Safety and Food Handling Practices. Foods, 10.","DOI":"10.3390\/foods10050907"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Wottlin, L.R., Harvey, R.B., Norman, K.N., Droleskey, R.E., Andrews, K., Jackson, S.J., Anderson, R.C., and Poole, T.L. (2024). Prevalence and Characterization of Salmonella during Pork Sausage Manufacturing. Microorganisms, 12.","DOI":"10.3390\/microorganisms12081599"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Papatzimos, G., Basdagianni, Z., and Kasapidou, E. (2024). Substitution of Animal Fat and Sodium Nitrite with Hemp Seed Oil: Effect on the Nutritional Value, Sensory Characteristics, and Shelf Life of Fermented Salami. Foods, 13.","DOI":"10.3390\/foods13162584"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"108432","DOI":"10.1016\/j.foodcont.2021.108432","article-title":"Enhancing the Reduction of Salmonella and Listeria monocytogenes during Traditional Salami Processing by Adding a Finishing Phase","volume":"131","author":"Mohamed","year":"2022","journal-title":"Food Control"},{"key":"ref_6","first-page":"31","article-title":"Quantitative Microbial Risk Assessment of Salmonella in Dry Fermented Sausage (Salami) in Southern Brazil","volume":"6","author":"Corbellini","year":"2017","journal-title":"Microb. Risk Anal."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"110933","DOI":"10.1016\/j.foodres.2021.110933","article-title":"Conventional and Emerging Approaches for Reducing Dietary Intake of Salt","volume":"152","author":"Vinitha","year":"2022","journal-title":"Food Res. Int."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"3223","DOI":"10.1038\/s41467-024-47526-8","article-title":"KdpD Is a Tandem Serine Histidine Kinase That Controls K+ Pump KdpFABC Transcriptionally and Post-Translationally","volume":"15","author":"Silberberg","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Rath, H., Reder, A., Hoffmann, T., Hammer, E., Seubert, A., Bremer, E., V\u00f6lker, U., and M\u00e4der, U. (2020). Management of Osmoprotectant Uptake Hierarchy in Bacillus subtilis via a SigB-Dependent Antisense RNA. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.00622"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Wang, H., Huang, M., Zeng, X., Peng, B., Xu, X., and Zhou, G. (2020). Resistance Profiles of Salmonella Isolates Exposed to Stresses and the Expression of Small Non-Coding RNAs. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.00130"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"11660","DOI":"10.1038\/s41598-024-62141-9","article-title":"Genomic Insights of Salmonella Isolated from Dry Fermented Sausage Production Chains in Spain and France","volume":"14","author":"Yvon","year":"2024","journal-title":"Sci. Rep."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"36088","DOI":"10.1021\/acsomega.3c04257","article-title":"Analysis of Osmotic Tolerance, Physiological Characteristics, and Gene Expression of Salmonella enterica Subsp. enterica Serotype Derby","volume":"8","author":"Li","year":"2023","journal-title":"ACS Omega"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"106540","DOI":"10.1016\/j.micpath.2024.106540","article-title":"Insight into the Inhibitory Activity and Mechanism of Bovine Cathelicidin BMAP 27 against Salmonella Typhimurium","volume":"187","author":"Xia","year":"2024","journal-title":"Microb. Pathog."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"115814","DOI":"10.1016\/j.lwt.2024.115814","article-title":"Antibacterial Mechanism of Slightly Acidic Electrolyzed Water against Pseudomonas arsenicoxydans A1 from Greater Amberjack (Seriola dumerili)","volume":"194","author":"Zhong","year":"2024","journal-title":"LWT"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"fyad068","DOI":"10.1093\/fqsafe\/fyad068","article-title":"Tolerance Variations and Mechanisms of Salmonella enterica Serovar Newport in Response to Long-Term Hypertonic Stress","volume":"8","author":"Zhang","year":"2024","journal-title":"Food Qual. Saf."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2749","DOI":"10.1038\/s41598-024-52538-x","article-title":"Evaluation of Antimicrobial Susceptibility Tests for Acinetobacter and Pseudomonas Species Using Disks Containing a High Dose of Meropenem","volume":"14","author":"Endo","year":"2024","journal-title":"Sci. Rep."},{"key":"ref_17","unstructured":"Clinical and Laboratory Standards Institute (CLSI) (2022). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [32nd ed.]. CLSI supplement M100."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"R599","DOI":"10.1016\/j.cub.2022.05.005","article-title":"Bacteria Grow Swiftly and Live Thriftily","volume":"32","author":"Kolter","year":"2022","journal-title":"Curr. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e01191-20","DOI":"10.1128\/mBio.01191-20","article-title":"Bacterial Evolution in High-Osmolarity Environments","volume":"11","author":"Cesar","year":"2020","journal-title":"mBio"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Hews, C.L., Cho, T., Rowley, G., and Raivio, T.L. (2019). Maintaining Integrity Under Stress: Envelope Stress Response Regulation of Pathogenesis in Gram-Negative Bacteria. Front. Cell. Infect. Microbiol., 9.","DOI":"10.3389\/fcimb.2019.00313"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Robertson, J., McGoverin, C., White, J.R., Vanholsbeeck, F., and Swift, S. (2021). Rapid Detection of Escherichia coli Antibiotic Susceptibility Using Live\/Dead Spectrometry for Lytic Agents. Microorganisms, 9.","DOI":"10.3390\/microorganisms9050924"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"122160","DOI":"10.1016\/j.carbpol.2024.122160","article-title":"Enhanced Photodynamic Inactivation against Escherichia coli O157:H7 Provided by Chitosan\/Curcumin Coating and Its Application in Food Contact Surfaces","volume":"337","author":"Zhang","year":"2024","journal-title":"Carbohydr. Polym."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Mandal, R.K., and Kwon, Y.M. (2017). Global Screening of Salmonella enterica Serovar Typhimurium Genes for Desiccation Survival. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.01723"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"166968","DOI":"10.1016\/j.jmb.2021.166968","article-title":"Molecular Mechanisms for Bacterial Potassium Homeostasis","volume":"433","author":"Stautz","year":"2021","journal-title":"J. Mol. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Liu, M., Liu, H., Mei, F., Yang, N., Zhao, D., Ai, G., Xiang, H., and Zheng, Y. (2022). Identification of the Biosynthetic Pathway of Glycine Betaine That Is Responsible for Salinity Tolerance in Halophilic Thioalkalivibrio Versutus D301. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.875843"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3383","DOI":"10.1038\/s41598-020-59231-9","article-title":"A Potassium Chloride to Glycine Betaine Osmoprotectant Switch in the Extreme Halophile Halorhodospira Halophila","volume":"10","author":"Deole","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"22196","DOI":"10.1074\/jbc.M910111199","article-title":"Extreme Halophiles Synthesize Betaine from Glycine by Methylation","volume":"275","author":"Kerovuo","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1093\/femsre\/fuy009","article-title":"Strategies of Adaptation of Microorganisms of the Three Domains of Life to High Salt Concentrations","volume":"42","author":"Oren","year":"2018","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1007\/BF00391761","article-title":"Regulation of Proline Utilization in Salmonella typhimurium: How Do Cells Avoid a Futile Cycle?","volume":"220","author":"Ekena","year":"1990","journal-title":"Mol. Gen. Genet. MGG"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"3861","DOI":"10.1128\/JB.00495-12","article-title":"Identification of a Third Osmoprotectant Transport System, the OsmU System, in Salmonella enterica","volume":"194","author":"Frossard","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/j.1574-6976.1994.tb00067.x","article-title":"Adaptation of Escherichia coli to High Osmolarity Environments: Osmoregulation of the High-Affinity Glycine Betaine Transport System ProU","volume":"14","author":"Lucht","year":"1994","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Lehman, M.K., Sturd, N.A., Razvi, F., Wellems, D.L., Carson, S.D., and Fey, P.D. (2023). Proline Transporters ProT and PutP Are Required for Staphylococcus aureus Infection. PLoS Pathog., 19.","DOI":"10.1371\/journal.ppat.1011098"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Vargas-Blanco, D.A., and Shell, S.S. (2020). Regulation of mRNA Stability During Bacterial Stress Responses. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.02111"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Heermann, R., Lippert, M.-L., and Jung, K. (2009). Domain Swapping Reveals That the N-Terminal Domain of the Sensor Kinase KdpD in Escherichia coli Is Important for Signaling. BMC Microbiol., 9.","DOI":"10.1186\/1471-2180-9-133"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1146\/annurev-micro-090110-102946","article-title":"The RpoS-Mediated General Stress Response in Escherichia coli","volume":"65","author":"Battesti","year":"2011","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"104943","DOI":"10.1016\/j.jbc.2023.104943","article-title":"Lack of Polyamines Leads to Cotranslational Degradation of the General Stress Factor RpoS in Escherichia coli","volume":"299","author":"Majdalani","year":"2023","journal-title":"J. Biol. Chem."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Krahulcov\u00e1, M., Cverenk\u00e1rov\u00e1, K., Olejn\u00edkov\u00e1, P., Micajov\u00e1, B., Korenekov\u00e1, J., and B\u00edro\u0161ov\u00e1, L. (2022). Characterization of Antibiotic Resistant Coliform Bacteria and Resistance Genes Isolated from Samples of Smoothie Drinks and Raw Milk. Foods, 11.","DOI":"10.3390\/foods11091324"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.foodcont.2018.12.043","article-title":"Phenotypic and Genotypic Characterization of Antimicrobial Resistant Escherichia coli Isolated from Ready-to-Eat Food in Singapore Using Disk Diffusion, Broth Microdilution and Whole Genome Sequencing Methods","volume":"99","author":"Guo","year":"2019","journal-title":"Food Control"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"112829","DOI":"10.1016\/j.ejmech.2020.112829","article-title":"\u03b2-Lactam Antibiotics: An Overview from a Medicinal Chemistry Perspective","volume":"208","author":"Lima","year":"2020","journal-title":"Eur. J. Med. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"e00724-21","DOI":"10.1128\/AEM.00724-21","article-title":"Extreme Acid Modulates Fitness Trade-Offs of Multidrug Efflux Pumps MdtEF-TolC and AcrAB-TolC in Escherichia coli K-12","volume":"87","author":"Schaffner","year":"2021","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"102170","DOI":"10.1016\/j.ceb.2023.102170","article-title":"Physiological and Regulatory Convergence between Osmotic and Nutrient Stress Responses in Microbes","volume":"81","author":"Brauer","year":"2023","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Wiktorczyk-Kapischke, N., Skowron, K., Grudlewska-Buda, K., Wa\u0142ecka-Zacharska, E., Korkus, J., and Gospodarek-Komkowska, E. (2021). Adaptive Response of Listeria monocytogenes to the Stress Factors in the Food Processing Environment. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.710085"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.ijbiomac.2021.02.081","article-title":"Biochemical Characterization of a Low Salt-Adapted Extracellular Protease from the Extremely Halophilic Archaeon Halococcus Salifodinae","volume":"176","author":"Hou","year":"2021","journal-title":"Int. J. Biol. Macromol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Ali, M.K., Li, X., Tang, Q., Liu, X., Chen, F., Xiao, J., Ali, M., Chou, S.-H., and He, J. (2017). Regulation of Inducible Potassium Transporter KdpFABC by the KdpD\/KdpE Two-Component System in Mycobacterium smegmatis. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.00570"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3266","DOI":"10.1111\/1462-2920.15087","article-title":"Impact of High Salinity and the Compatible Solute Glycine Betaine on Gene Expression of Bacillus subtilis","volume":"22","author":"Rath","year":"2020","journal-title":"Environ. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"110089","DOI":"10.1016\/j.lwt.2020.110089","article-title":"Collateral Adaptive Responses Induced by Desiccation Stress in Salmonella enterica","volume":"133","author":"Abdelhamid","year":"2020","journal-title":"LWT"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"100989","DOI":"10.1016\/j.onehlt.2025.100989","article-title":"Disinfectants and One Health Review: The Role of Reactive Oxygen Species in the Bactericidal Activity of Chlorine against Salmonella","volume":"20","author":"Aljuwayd","year":"2025","journal-title":"One Health"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"976","DOI":"10.1080\/10408398.2018.1555132","article-title":"Salmonella enterica: A Hidden Risk for Dry-Cured Meat Consumption?","volume":"60","author":"Mutz","year":"2020","journal-title":"Crit. Rev. Food Sci. Nutr."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"111955","DOI":"10.1016\/j.foodres.2022.111955","article-title":"Overview of Antimicrobial Resistance and Virulence Factors in Salmonella spp. Isolated in the Last Two Decades from Chicken in Brazil","volume":"162","author":"Morasi","year":"2022","journal-title":"Food Res. Int."}],"container-title":["Foods"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2304-8158\/14\/9\/1440\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:19:02Z","timestamp":1760030342000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2304-8158\/14\/9\/1440"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,4,22]]},"references-count":49,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["foods14091440"],"URL":"https:\/\/doi.org\/10.3390\/foods14091440","relation":{},"ISSN":["2304-8158"],"issn-type":[{"value":"2304-8158","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,4,22]]}}}