{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T03:10:13Z","timestamp":1791083413015,"version":"4.1.0"},"reference-count":42,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,3,10]],"date-time":"2022-03-10T00:00:00Z","timestamp":1646870400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,3,10]],"date-time":"2022-03-10T00:00:00Z","timestamp":1646870400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001731","name":"Danida Fellowship Centre","doi-asserted-by":"publisher","award":["14-P01-TAN"],"award-info":[{"award-number":["14-P01-TAN"]}],"id":[{"id":"10.13039\/501100001731","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Non-<jats:italic>enterica<\/jats:italic> subspecies of <jats:italic>Salmonella enterica<\/jats:italic> are rarely associated with human infections. Paradoxically, food safety legislations consider the entire genus <jats:italic>Salmonella<\/jats:italic> as pathogenic to humans. Globally, large amounts of seafoods are rejected and wasted due to findings of <jats:italic>Salmonella<\/jats:italic>. To inform better food safety decisions, we investigated the pathogenicity of <jats:italic>Salmonella<\/jats:italic> Salamae 42:r- and <jats:italic>Salmonella<\/jats:italic> Waycross isolated from Nile perch from Lake Victoria. Genome-wide analysis revealed absence of significant virulence determinants including on key <jats:italic>Salmonella<\/jats:italic> pathogenicity islands in both serovars. In epithelial cells, <jats:italic>S.<\/jats:italic> Salamae showed a weak invasion ability that was lower than the <jats:italic>invH<\/jats:italic> mutant of <jats:italic>S.<\/jats:italic> Typhimiurium used as negative control. Similarly, <jats:italic>S<\/jats:italic>. Salamae could not replicate inside macrophages. Moreover, intracellular replication in <jats:italic>S.<\/jats:italic> Waycross strains was significantly lower compared to the wild type <jats:italic>S.<\/jats:italic> Typhimurium. Our findings suggest a low pathogenicity of <jats:italic>S<\/jats:italic>. Salamae reinforcing the existing literature that non-<jats:italic>enterica<\/jats:italic> subspecies are avirulent. We propose that food legislations and actions taken on findings of <jats:italic>Salmonella<\/jats:italic> are revisited to avoid wasting valuable sea- and other foods.<\/jats:p>","DOI":"10.1038\/s41598-022-08200-5","type":"journal-article","created":{"date-parts":[[2022,3,10]],"date-time":"2022-03-10T17:05:23Z","timestamp":1646931923000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Salmonella Salamae and S. Waycross isolated from Nile perch in Lake Victoria show limited human pathogenic potential"],"prefix":"10.1038","volume":"12","author":[{"given":"Yaovi Mahuton Gildas","family":"Hounmanou","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zebedayo","family":"Baniga","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vanesa","family":"Garc\u00eda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anders","family":"Dalsgaard","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,3,10]]},"reference":[{"key":"8200_CR1","doi-asserted-by":"publisher","first-page":"e1752","DOI":"10.7717\/peerj.1752","volume":"4","author":"PM Ashton","year":"2016","unstructured":"Ashton, P. M. et al. Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ 4, e1752 (2016).","journal-title":"PeerJ"},{"key":"8200_CR2","doi-asserted-by":"publisher","DOI":"10.5772\/30812","volume-title":"Salmonella\u2014A Dangerous Foodborne Pathogen","author":"ENC Tessari","year":"2012","unstructured":"Tessari, E. N. C. et al. Important aspects of Salmonella in the poultry industry and in public health. In Salmonella\u2014A Dangerous Foodborne Pathogen (ed. Barakat, S. M.) (InTech, 2012). https:\/\/doi.org\/10.5772\/30812."},{"key":"8200_CR3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3855\/jidc.56","volume":"3","author":"OM David","year":"2009","unstructured":"David, O. M., Wandili, S., Kakai, R. & Waindi, E. N. Isolation of Salmonella and Shigella from fish harvested from the Winam Gulf of Lake Victoria, Kenya. J. Inf. Dev. Ctries. 3, 1. https:\/\/doi.org\/10.3855\/jidc.56 (2009).","journal-title":"J. Inf. Dev. Ctries."},{"key":"8200_CR4","first-page":"18087","volume":"7","author":"RH Mdegela","year":"2015","unstructured":"Mdegela, R. H., Mhongole, O. J., Kamundia, P. W., Byarugaba, D. & Mbuthia, P. G. Identification of Salmonella and Vibrio in water and Oreochromis niloticus in Mwanza Gulf, Lake Victoria, Tanzania. Int. J. Curr. Res. 7, 18087\u201318092 (2015).","journal-title":"Int. J. Curr. Res."},{"key":"8200_CR5","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/j.marpolbul.2015.04.032","volume":"95","author":"VR Prasad","year":"2015","unstructured":"Prasad, V. R., Srinivas, T. N. R. & Sarma, V. V. S. S. Influence of river discharge on abundance and dissemination of heterotrophic, indicator and pathogenic bacteria along the east coast of India. Mar. Pollut. Bull. 95, 115\u2013125 (2015).","journal-title":"Mar. Pollut. Bull."},{"key":"8200_CR6","doi-asserted-by":"publisher","first-page":"2465","DOI":"10.1128\/JCM.38.7.2465-2467.2000","volume":"38","author":"FW Brenner","year":"2000","unstructured":"Brenner, F. W., Villar, R. G., Angulo, F. J., Tauxe, R. & Swaminathan, B. Salmonella nomenclature. J. Clin. Microbiol. 38, 2465\u20132467 (2000).","journal-title":"J. Clin. Microbiol."},{"key":"8200_CR7","doi-asserted-by":"publisher","first-page":"831","DOI":"10.1099\/jmm.0.072702-0","volume":"63","author":"S Nair","year":"2014","unstructured":"Nair, S., Wain, J., Connell, S., de Pinna, E. & Peters, T. Salmonella enterica subspecies II infections in England and Wales\u2014The use of multilocus sequence typing to assist serovar identification. J. Med. Microbiol. 63, 831\u2013834 (2014).","journal-title":"J. Med. Microbiol."},{"key":"8200_CR8","doi-asserted-by":"publisher","first-page":"456","DOI":"10.17221\/44\/2017-VETMED","volume":"62","author":"Z Tomastikova","year":"2017","unstructured":"Tomastikova, Z., Barazorda Romero, S., Knotek, Z. & Karpiskova, R. Prevalence and characteristics of Salmonella species isolated from captive reptiles in the Czech Republic. Vet. Med. 62, 456\u2013469 (2017).","journal-title":"Vet. Med."},{"key":"8200_CR9","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00591-19","author":"RG Ferrari","year":"2019","unstructured":"Ferrari, R. G. et al. Worldwide epidemiology of Salmonella Serovars in animal-based foods: A meta-analysis. Appl. Environ. Microbiol. https:\/\/doi.org\/10.1128\/AEM.00591-19 (2019).","journal-title":"Appl. Environ. Microbiol."},{"key":"8200_CR10","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.01985","author":"YMG Hounmanou","year":"2020","unstructured":"Hounmanou, Y. M. G. et al. Molecular characteristics and zoonotic potential of Salmonella Weltevreden from cultured Shrimp and Tilapia in Vietnam and China. Front. Microbiol. https:\/\/doi.org\/10.3389\/fmicb.2020.01985 (2020).","journal-title":"Front. Microbiol."},{"key":"8200_CR11","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1016\/j.foodcont.2019.01.006","volume":"100","author":"Z Baniga","year":"2019","unstructured":"Baniga, Z., Mdegela, R. H., Lisa, B., Kusiluka, L. J. M. & Dalsgaard, A. Prevalence and characterisation of Salmonella Waycross and Salmonella enterica subsp. salamae in Nile perch (Lates niloticus) of Lake Victoria, Tanzania. Food Control 100, 28\u201334 (2019).","journal-title":"Food Control"},{"key":"8200_CR12","first-page":"79","volume":"1","author":"D Mungai","year":"2002","unstructured":"Mungai, D., Mwatha, W. E. & Okemo, P. Salmonella and Vibrio cholerae in Nile perch (Lates niloticus) processing establishments in Kenya. J. Trop. Microbiol. Biotechnol. 1, 79\u201388 (2002).","journal-title":"J. Trop. Microbiol. Biotechnol."},{"key":"8200_CR13","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1016\/j.micres.2017.09.010","volume":"206","author":"A Lamas","year":"2018","unstructured":"Lamas, A. et al. A comprehensive review of non-enterica subspecies of Salmonella enterica. Microbiol. Res. 206, 60\u201373 (2018).","journal-title":"Microbiol. Res."},{"key":"8200_CR14","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1186\/1471-2180-13-253","volume":"13","author":"A Kagamb\u00e8ga","year":"2013","unstructured":"Kagamb\u00e8ga, A. et al. Prevalence and characterization of Salmonella enterica from the feces of cattle, poultry, swine and hedgehogs in Burkina Faso and their comparison to human Salmonella isolates. BMC Microbiol. 13, 253 (2013).","journal-title":"BMC Microbiol."},{"key":"8200_CR15","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1016\/j.ijfoodmicro.2008.01.007","volume":"123","author":"A Stevens","year":"2008","unstructured":"Stevens, A. et al. Epidemiological analysis of Salmonella enterica from beef sampled in the slaughterhouse and retailers in Dakar (Senegal) using pulsed-field gel electrophoresis and antibiotic susceptibility testing. Int. J. Food Microbiol. 123, 191\u2013197 (2008).","journal-title":"Int. J. Food Microbiol."},{"key":"8200_CR16","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.00198-13","author":"PT Desai","year":"2013","unstructured":"Desai, P. T. et al. Evolutionary genomics of Salmonella enterica subspecies. MBio https:\/\/doi.org\/10.1128\/mBio.00198-13 (2013).","journal-title":"MBio"},{"key":"8200_CR17","doi-asserted-by":"publisher","first-page":"1056","DOI":"10.1099\/mic.0.047001-0","volume":"157","author":"E Gan","year":"2011","unstructured":"Gan, E., Baird, F. J., Coloe, P. J. & Smooker, P. M. Phenotypic and molecular characterization of Salmonella enterica serovar Sofia, an avirulent species in Australian poultry. Microbiology 157, 1056\u20131065 (2011).","journal-title":"Microbiology"},{"key":"8200_CR18","doi-asserted-by":"publisher","first-page":"2843","DOI":"10.1128\/JB.01223-08","volume":"191","author":"E Katribe","year":"2009","unstructured":"Katribe, E., Bogomolnaya, L. M., Wingert, H. & Andrews-Polymenis, H. Subspecies IIIa and IIIb Salmonellae are defective for colonization of Murine models of Salmonellosis compared to Salmonella enterica subsp. I Serovar Typhimurium. J. Bacteriol. 191, 2843\u20132850 (2009).","journal-title":"J. Bacteriol."},{"key":"8200_CR19","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2019.00270","author":"L Lou","year":"2019","unstructured":"Lou, L., Zhang, P., Piao, R. & Wang, Y. Salmonella Pathogenicity Island 1 (SPI-1) and its complex regulatory network. Front. Cell. Infect. Microbiol. https:\/\/doi.org\/10.3389\/fcimb.2019.00270 (2019).","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"8200_CR20","doi-asserted-by":"publisher","first-page":"1793","DOI":"10.1128\/AEM.02033-08","volume":"75","author":"B Bleasdale","year":"2009","unstructured":"Bleasdale, B. et al. The Salmonella pathogenicity Island 2-encoded type III secretion system is essential for the survival of Salmonella enterica Serovar Typhimurium in free-living Amoebae. Appl. Environ. Microbiol. 75, 1793\u20131795 (2009).","journal-title":"Appl. Environ. Microbiol."},{"key":"8200_CR21","doi-asserted-by":"publisher","first-page":"3618","DOI":"10.1128\/IAI.00704-16","volume":"84","author":"DJ Pollard","year":"2016","unstructured":"Pollard, D. J. et al. The type III secretion system effector SeoC of Salmonella enterica subsp. salamae and S. enterica subsp. arizonae ADP-ribosylates Src and inhibits opsonophagocytosis. Infect. Immun. 84, 3618\u20133628 (2016).","journal-title":"Infect. Immun."},{"key":"8200_CR22","doi-asserted-by":"publisher","first-page":"1216","DOI":"10.3389\/fmicb.2015.01216","volume":"6","author":"JL Balc\u00e1zar","year":"2015","unstructured":"Balc\u00e1zar, J. L., Subirats, J. & Borrego, C. M. The role of biofilms as environmental reservoirs of antibiotic resistance. Front. Microbiol. 6, 1216 (2015).","journal-title":"Front. Microbiol."},{"key":"8200_CR23","volume-title":"Antigenic Formulae of the Salmonella serovar","author":"PAD Grimont","year":"2007","unstructured":"Grimont, P. A. D. & Weill, F.-X. Antigenic Formulae of the Salmonella serovar (Institut Pasteur, 2007)."},{"key":"8200_CR24","doi-asserted-by":"publisher","first-page":"e0185056","DOI":"10.1371\/journal.pone.0185056","volume":"12","author":"B Bushnell","year":"2017","unstructured":"Bushnell, B., Rood, J. & Singer, E. BBMerge\u2014Accurate paired shotgun read merging via overlap. PLoS ONE 12, e0185056 (2017).","journal-title":"PLoS ONE"},{"key":"8200_CR25","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1089\/cmb.2012.0021","volume":"19","author":"A Bankevich","year":"2012","unstructured":"Bankevich, A. et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455\u2013477 (2012).","journal-title":"J. Comput. Biol."},{"key":"8200_CR26","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1093\/bioinformatics\/btt086","volume":"29","author":"A Gurevich","year":"2013","unstructured":"Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 29, 1072\u20131075 (2013).","journal-title":"Bioinformatics"},{"key":"8200_CR27","doi-asserted-by":"publisher","first-page":"1685","DOI":"10.1128\/JCM.00323-15","volume":"53","author":"S Zhang","year":"2015","unstructured":"Zhang, S. et al. Salmonella serotype determination utilizing high-throughput genome sequencing data. J. Clin. Microbiol. 53, 1685\u20131692 (2015).","journal-title":"J. Clin. Microbiol."},{"key":"8200_CR28","doi-asserted-by":"publisher","first-page":"e1002776","DOI":"10.1371\/journal.ppat.1002776","volume":"8","author":"M Achtman","year":"2012","unstructured":"Achtman, M. et al. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog. 8, e1002776 (2012).","journal-title":"PLoS Pathog."},{"key":"8200_CR29","doi-asserted-by":"publisher","first-page":"3895","DOI":"10.1128\/AAC.02412-14","volume":"58","author":"A Carattoli","year":"2014","unstructured":"Carattoli, A. et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895\u20133903 (2014).","journal-title":"Antimicrob. Agents Chemother."},{"key":"8200_CR30","doi-asserted-by":"publisher","first-page":"2640","DOI":"10.1093\/jac\/dks261","volume":"67","author":"E Zankari","year":"2012","unstructured":"Zankari, E. et al. Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640\u20132644 (2012).","journal-title":"J. Antimicrob. Chemother."},{"key":"8200_CR31","doi-asserted-by":"publisher","first-page":"W16","DOI":"10.1093\/nar\/gkw387","volume":"44","author":"D Arndt","year":"2016","unstructured":"Arndt, D. et al. PHASTER: A better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16-21 (2016).","journal-title":"Nucleic Acids Res."},{"key":"8200_CR32","doi-asserted-by":"publisher","first-page":"D624","DOI":"10.1093\/nar\/gku985","volume":"43","author":"SH Yoon","year":"2015","unstructured":"Yoon, S. H., Park, Y.-K. & Kim, J. F. PAIDB v2.0: Exploration and analysis of pathogenicity and resistance islands. Nucleic Acids Res. 43, D624\u2013D630 (2015).","journal-title":"Nucleic Acids Res."},{"key":"8200_CR33","doi-asserted-by":"publisher","first-page":"3422","DOI":"10.1093\/bioinformatics\/bti553","volume":"21","author":"TJ Carver","year":"2005","unstructured":"Carver, T. J. et al. ACT: The Artemis Comparison Tool. Bioinformatics 21, 3422\u20133423 (2005).","journal-title":"Bioinformatics"},{"key":"8200_CR34","doi-asserted-by":"publisher","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","volume":"30","author":"T Seemann","year":"2014","unstructured":"Seemann, T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 30, 2068\u20132069 (2014).","journal-title":"Bioinformatics"},{"key":"8200_CR35","doi-asserted-by":"publisher","first-page":"3691","DOI":"10.1093\/bioinformatics\/btv421","volume":"31","author":"AJ Page","year":"2015","unstructured":"Page, A. J. et al. Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691\u20133693 (2015).","journal-title":"Bioinformatics"},{"key":"8200_CR36","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1186\/s13059-016-1108-8","volume":"17","author":"O Brynildsrud","year":"2016","unstructured":"Brynildsrud, O., Bohlin, J., Scheffer, L. & Eldholm, V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary. Genome Biol. 17, 238 (2016).","journal-title":"Genome Biol."},{"key":"8200_CR37","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1093\/bioinformatics\/btx610","volume":"34","author":"J Hadfield","year":"2018","unstructured":"Hadfield, J. et al. Phandango: An interactive viewer for bacterial population genomics. Bioinformatics 34, 292\u2013293 (2018).","journal-title":"Bioinformatics"},{"key":"8200_CR38","doi-asserted-by":"publisher","first-page":"D286","DOI":"10.1093\/nar\/gkv1248","volume":"44","author":"J Huerta-Cepas","year":"2016","unstructured":"Huerta-Cepas, J. et al. eggNOG 4.5: A hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44, D286\u2013D293 (2016).","journal-title":"Nucleic Acids Res"},{"key":"8200_CR39","first-page":"566","volume":"19","author":"J Li","year":"2018","unstructured":"Li, J. et al. VRprofile: Gene-cluster-detection-based profiling of virulence and antibiotic resistance traits encoded within genome sequences of pathogenic bacteria. Brief Bioinform. 19, 566\u2013574 (2018).","journal-title":"Brief Bioinform."},{"key":"8200_CR40","doi-asserted-by":"publisher","first-page":"e104984","DOI":"10.1371\/journal.pone.0104984","volume":"9","author":"RS Kaas","year":"2014","unstructured":"Kaas, R. S., Leekitcharoenphon, P., Aarestrup, F. M. & Lund, O. Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS ONE 9, e104984 (2014).","journal-title":"PLoS ONE"},{"key":"8200_CR41","doi-asserted-by":"publisher","first-page":"D206","DOI":"10.1093\/nar\/gkt1226","volume":"42","author":"R Overbeek","year":"2014","unstructured":"Overbeek, R. et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 42, D206-214 (2014).","journal-title":"Nucleic Acids Res."},{"key":"8200_CR42","doi-asserted-by":"publisher","first-page":"e00784-17","DOI":"10.1128\/IAI.00784-17","volume":"86","author":"A Herrero-Fresno","year":"2018","unstructured":"Herrero-Fresno, A. et al. The homolog of the gene bstA of the BTP1 phage from Salmonella enterica Serovar Typhimurium ST313 is an Antivirulence Gene in Salmonella enterica Serovar Dublin. Infect. Immun. 86, e00784-17 (2018).","journal-title":"Infect. Immun."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-08200-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-08200-5","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-08200-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,25]],"date-time":"2022-11-25T00:23:27Z","timestamp":1669335807000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-08200-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,10]]},"references-count":42,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["8200"],"URL":"https:\/\/doi.org\/10.1038\/s41598-022-08200-5","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,10]]},"assertion":[{"value":"15 December 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 March 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 March 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"4229"}}