{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,27]],"date-time":"2026-08-27T20:29:42Z","timestamp":1787862582619,"version":"build-2784847793"},"reference-count":81,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2024,9,10]],"date-time":"2024-09-10T00:00:00Z","timestamp":1725926400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>The cluster of genes determining the production of botulinum toxins is an attribute of not only the Clostridium botulinum species. This cluster is also found in other members of the Clostridium genus, such as C. baratii, C. butyricum, and C. sporogenes. The occurrence of a botulinum-like cluster has also been recorded in strains of other genera, i.e., Enterococcus faecium, as well as in a Gram-negative species isolated from freshwater sediments; however, the biological activity of bont-related genes has not been noted. It can be said that the mentioned species have a dual nature. Another species with a dual nature is C. butyricum. This bacterium is a common human and animal gut commensal bacterium and is also frequently found in the environment. Although non-toxigenic strains are currently used as probiotics in Asia, other strains have been implicated in pathological conditions, such as botulism in infants or necrotizing enterocolitis in preterm neonates. Additionally, C. baratii strains are rare opportunistic pathogens associated with botulism intoxication. They have been isolated from food and soil and can be carried asymptomatically or cause botulism outbreaks in animals and humans. In addition to the mentioned clostridia, the other microorganisms considered as non-toxigenic have also been suspected of carrying botulinum cluster Gram-negative bacteria, such as Chryseobacterium piperi isolated from freshwater sediments; however, the biological activity of bont-related genes has not been noted. Additionally, Enterococcus faecium strains have been discovered carrying BoNT-related clusters (BoNT\/En). Literature data regarding the heterogeneity of BoNT-producing strains indicate the requirement to reclassify C. botulinum species and other microorganisms able to produce BoNTs or possess botulinum-like gene clusters. This article aims to show the dual nature of Clostridium strains not belonging to the C. botulinum species that are sporadically able to carry bont clusters, which are usually considered saprophytic and even probiotic, and bont-like clusters in microorganisms from other genera. The aim was also to consider the genetic mechanisms of botulinum cluster expression in strains that are considered opportunistic and the microbiological safety aspects associated with their occurrence in the environment.<\/jats:p>","DOI":"10.3390\/pathogens13090780","type":"journal-article","created":{"date-parts":[[2024,9,10]],"date-time":"2024-09-10T10:20:10Z","timestamp":1725963610000},"page":"780","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Opportunistic Features of Non-Clostridium botulinum Strains Containing bont Gene Cluster"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4619-128X","authenticated-orcid":false,"given":"Tomasz","family":"Grenda","sequence":"first","affiliation":[{"name":"Department of Hygiene of Animal Feeding Stuffs, National Veterinary Research Institute in Pulawy, Patyzantow 57, 24-100 Pulawy, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Grenda","sequence":"additional","affiliation":[{"name":"Department of Pneumonology, Oncology and Allergology, Medical University in Lublin, ul. Jaczewskiego 8, 20-090 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1087-2000","authenticated-orcid":false,"given":"Anna","family":"Jakubczyk","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Food Chemistry, University of Life Sciences in Lublin, Skromna 8, 20-704 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2100-1315","authenticated-orcid":false,"given":"Kamila","family":"Rybczy\u0144ska-Tkaczyk","sequence":"additional","affiliation":[{"name":"Department of Environmental Microbiology, University of Life Sciences in Lublin, St. Leszczy\u0144skiego 7, 20-069 Lublin, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,9,10]]},"reference":[{"key":"ref_1","first-page":"515","article-title":"Beneficial and harmful roles of bacteria from the Clostridium genus","volume":"60","author":"Samul","year":"2013","journal-title":"Acta Biochim. Pol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Guo, P., Zhang, K., Ma, X., and He, P. (2020). Clostridium species as probiotics: Potentials and challenges. J. Anim. Sci. Biotechnol., 11.","DOI":"10.1186\/s40104-019-0402-1"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1007\/s00702-007-0728-2","article-title":"From poison to remedy: The chequered history of botulinum toxin","volume":"115","author":"Erbguth","year":"2008","journal-title":"J. Neural Transm."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1128\/iai.5.6.985-986.1972","article-title":"Cryoprotein produced by Clostridium botulinum type G","volume":"5","author":"Ciccarelli","year":"1972","journal-title":"Infect. Immun."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Minton, N.P., and Clarke, D.J. (1989). Taxonomy and Phylogeny. Clostridia, Springer.","DOI":"10.1007\/978-1-4757-9718-3"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.resmic.2014.10.010","article-title":"Genomes, neurotoxins and biology of Clostridium botulinum Group I and Group II","volume":"166","author":"Carter","year":"2015","journal-title":"Res. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1046\/j.1365-2672.1997.00313.x","article-title":"Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins","volume":"84","author":"Collins","year":"1998","journal-title":"J. Appl. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Scalfaro, C., Iacobino, A., Grande, L., Morabito, S., and Franciosa, G. (2016). Effects of megaplasmid loss on growth of neurotoxigenic Clostridium butyricum strains and botulinum neurotoxin type E expression. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.00217"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1002\/1873-3468.12969","article-title":"Identification of a novel botulinum neurotoxin gene cluster in Enterococcus","volume":"592","author":"Brunt","year":"2018","journal-title":"FEBS Lett."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e941731","DOI":"10.12659\/AJCR.941731","article-title":"Unusual Case of Ludwig Angina Caused by Clostridium sporogenes in an Immunocompromised HIV-Positive Patient with Alcoholism and Dental Abscess","volume":"24","author":"Truong","year":"2023","journal-title":"Am. J. Case Rep."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Lorenzo, J.M., Munekata, P.E., Dominguez, R., Pateiro, M., Saraiva, J.A., and Franco, D. (2018). Main Groups of Microorganisms of Relevance for Food Safety and Stability: General Aspects and Overall Description, Elsevier.","DOI":"10.1016\/B978-0-12-811031-7.00003-0"},{"key":"ref_12","first-page":"95","article-title":"Clostridium Sporogenes Causing Bacteremia Originated from the Skin and Soft Tissue Infection in an Immunocompetent Patient\u2014Case Report and Literature Review","volume":"6","author":"Alataby","year":"2020","journal-title":"Int. J. Crit. Care Emerg. Med."},{"key":"ref_13","first-page":"8812635","article-title":"Cognitive Biases in the Era of COVID-19: A Case of Clostridium sporogenes Bacteremia in a Patient with Small Bowel Obstruction","volume":"2020","author":"Vecchio","year":"2020","journal-title":"Case Rep. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1928","DOI":"10.1002\/1097-0142(19910401)67:7<1928::AID-CNCR2820670718>3.0.CO;2-9","article-title":"Clostridial bacteremia in cancer patients. A 12-year experience","volume":"67","author":"Bodey","year":"1991","journal-title":"Cancer"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e00481","DOI":"10.1016\/j.idcr.2018.e00481","article-title":"Clostridium sporogenes bacteremia in an immunocompetent patient","volume":"15","author":"Abusnina","year":"2019","journal-title":"IDCases"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1086\/321883","article-title":"Clinical features of clostridial bacteremia: A review from a rural area","volume":"33","author":"Rechner","year":"2001","journal-title":"Clin. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1097\/MRM.0b013e328362fa5b","article-title":"Septicaemia caused by Clostridium sporogenes: Two case reports and a literature review","volume":"24","author":"Shen","year":"2013","journal-title":"Rev. Res. Med. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"217","DOI":"10.37201\/req\/111.2022","article-title":"Bacteremia caused by Clostridium sporogenes in an oncological patient","volume":"36","author":"Cobo","year":"2023","journal-title":"Rev. Esp. Quimioter."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"102202","DOI":"10.1016\/j.anaerobe.2020.102202","article-title":"Clinical relevance of Clostridium bacteremia: An 8-year retrospective study","volume":"63","author":"Stabler","year":"2020","journal-title":"Anaerobe"},{"key":"ref_20","first-page":"242","article-title":"Empyema With Hydropneumothorax and Bacteremia Caused by Clostridium sporogenes","volume":"312","author":"Corbett","year":"1996","journal-title":"Am. J. Med. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"155","DOI":"10.3109\/inf.1970.2.issue-2.14","article-title":"Case report: Primary thoracic empyema caused by clostridium sporogenes","volume":"2","author":"Malmborg","year":"1970","journal-title":"Scand. J. Infect. Dis."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"820","DOI":"10.1136\/jcp.2010.084434","article-title":"Septic arthritis following anterior cruciate ligament reconstruction secondary to Clostridium sporogenes; a rare clinical pathogen","volume":"64","author":"Inkster","year":"2011","journal-title":"J. Clin. Pathol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1016\/S0039-6109(16)40800-5","article-title":"Gangrene infection: New approaches to an old disease","volume":"55","author":"Hitchcock","year":"1975","journal-title":"Surg. Clin. N. Am."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1016\/S1473-3099(20)30024-4","article-title":"Non-traumatic gas gangrene due to Clostridium sporogenes","volume":"20","author":"Kanaujia","year":"2020","journal-title":"Lancet Infect. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1080\/23744235.2019.1696472","article-title":"The antibiotic susceptibility pattern of gas gangrene-forming Clostridium spp. clinical isolates from South-Eastern Hungary","volume":"52","author":"Schoblocher","year":"2020","journal-title":"Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1006\/bbrc.1996.1521","article-title":"Purification and some properties of Clostridium sporogenes hemorrhagic toxin","volume":"227","author":"Yamakawa","year":"1996","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Brunt, J., van Vliet, A.H.M., Carter, A.T., Stringer, S.C., Amar, C., Grant, K.A., Godbole, G., and Peck, M.W. (2020). Diversity of the Genomes and Neurotoxins of Strains of Clostridium botulinum Group I and Clostridium sporogenes Associated with Foodborne, Infant and Wound Botulism. Toxins, 12.","DOI":"10.3390\/toxins12090586"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Williamson, C.H.D., Sahl, J.W., Smith, T.J., Xie, G., Foley, B.T., Smith, L.A., Fern\u00e1ndez, R.A., Lindstr\u00f6m, M., Korkeala, H., and Keim, P. (2016). Comparative genomic analyses reveal broad diversity in botulinum-toxinproducing Clostridia. BMC Genom., 17.","DOI":"10.1186\/s12864-016-2502-z"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1643","DOI":"10.1093\/gbe\/evw101","article-title":"Diversity of group i and II clostridium botulinum strains from France including recently identified subtypes","volume":"8","author":"Mazuet","year":"2016","journal-title":"Genome Biol. Evol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.resmic.2014.09.007","article-title":"Historical and current perspectives on Clostridium botulinum diversity","volume":"166","author":"Smith","year":"2015","journal-title":"Res. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.meegid.2015.08.042","article-title":"Genomic characterization of Italian Clostridium botulinum group I strains","volume":"36","author":"Giordani","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1093\/pubmed\/fdl053","article-title":"Food-borne botulism in the United Kingdom","volume":"28","author":"McLauchlin","year":"2006","journal-title":"J. Public Health"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Franciosa, G., Maugliani, A., Scalfaro, C., and Aureli, P. (2009). Evidence that plasmid-borne botulinum neurotoxin type B genes are widespread among Clostridium botulinum serotype B strains. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0004829"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Liberato, V., Benevenuti, C., Coelho, F., Botelho, A., Amaral, P., Pereira, N., and Ferreira, T. (2019). Clostridium sp. as Bio-Catalyst for Fuels and Chemicals Production in a Biorefinery Context. Catalysts, 9.","DOI":"10.3390\/catal9110962"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Mo\u021b\u0103\u021b\u0103ianu, A., \u0218erban, G., and Andone, S. (2023). The Role of Short-Chain Fatty Acids in Microbiota-Gut-Brain Cross-Talk with a Focus on Amyotrophic Lateral Sclerosis: A Systematic Review. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms242015094"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Gao, X., Liu, X., Wang, Y., Wang, T., Fang, D., and Hu, K. (2023). Effects of Clostridium butyricum on Intestinal Microflora and Metabolism of Eriocheir sinensis. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms241813784"},{"key":"ref_37","unstructured":"European Commission (2014). Commission Implementing Decision of 10 March 2014. Off. J. Eur. Union, 588, 30\u201333."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Ariyoshi, T., Hagihara, M., Takahashi, M., and Mikamo, H. (2022). Effect of Clostridium butyricum on Gastrointestinal Infections. Biomedicines, 10.","DOI":"10.3390\/biomedicines10020483"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1046\/j.1442-200X.2003.01671.x","article-title":"Prevention of antibiotic-associated diarrhea in children by Clostridium butyricum MIYAIRI","volume":"45","author":"Seki","year":"2003","journal-title":"Pediatr. Int."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"100772","DOI":"10.1016\/j.isci.2019.100772","article-title":"Clostridium butyricum Modulates the Microbiome to Protect Intestinal Barrier Function in Mice with Antibiotic-Induced Dysbiosis","volume":"23","author":"Hagihara","year":"2020","journal-title":"iScience"},{"key":"ref_41","first-page":"1","article-title":"Growth stimulation of Clostridium butyricum in the presence of Lactobacillus brevis JL16 and Lactobacillus parabuchneri MH44","volume":"42","author":"So","year":"2022","journal-title":"Food Sci. Technol. Braz."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1186\/s12967-024-05031-y","article-title":"Gut microbiota dynamics and fecal SCFAs after colonoscopy: Accelerating microbiome stabilization by Clostridium butyricum","volume":"22","author":"Chen","year":"2024","journal-title":"J. Transl. Med."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Zhang, M., Zhang, Z., Zhang, X., Lu, C., Yang, W., Xie, X., Xin, H., Lu, X., Ni, M., and Yang, X. (2024). Effects of dietary Clostridium butyricum and rumen protected fat on meat quality, oxidative stability, and chemical composition of finishing goats. J. Anim. Sci. Biotechnol., 15.","DOI":"10.1186\/s40104-023-00972-8"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Zhang, X., Yun, Y., Lai, Z., Ji, S., Yu, G., Xie, Z., Zhang, H., Zhong, X., Wang, T., and Zhang, L. (2023). Supplemental Clostridium butyricum modulates lipid metabolism by reshaping the gut microbiota composition and bile acid profile in IUGR suckling piglets. J. Anim. Sci. Biotechnol., 14.","DOI":"10.1186\/s40104-023-00828-1"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4717","DOI":"10.1007\/s10499-024-01398-3","article-title":"Analyzing the influence of Clostridium butyricum on liver health in spotted sea bass (Lateolabrax maculatus) via transcriptomics and metabolomics","volume":"32","author":"Kong","year":"2024","journal-title":"Aquac. Int."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Liao, J., Liu, Y., Pei, Z., Wang, H., Zhu, J., Zhao, J., Lu, W., and Chen, W. (2023). Clostridium butyricum Reduces Obesity in a Butyrate-Independent Way. Microorganisms, 11.","DOI":"10.3390\/microorganisms11051292"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Liao, J., Liu, Y., Yao, Y., Zhang, J., Wang, H., Zhao, J., Chen, W., and Lu, W. (2023). Clostridium butyricum Strain CCFM1299 Reduces Obesity via Increasing Energy Expenditure and Modulating Host Bile Acid Metabolism. Nutrients, 15.","DOI":"10.3390\/nu15204339"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Tayyib, H.M.U., Ali, A., Jabeen, S., Kamran, H., Bajaber, M.A., Usman, M., and Zhang, X. (2024). Restoration of gut dysbiosis through Clostridium butyricum and magnesium possibly balance blood glucose levels: An experimental study. BMC Microbiol., 24.","DOI":"10.1186\/s12866-024-03218-3"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"390","DOI":"10.4093\/dmj.2023.0109","article-title":"Supplementation of Clostridium butyricum Alleviates Vascular Inflammation in Diabetic Mice","volume":"48","author":"Zhou","year":"2024","journal-title":"Diabetes Metab. J."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1038\/s41409-024-02250-1","article-title":"Clostridium butyricum MIYAIRI 588 contributes to the maintenance of intestinal microbiota diversity early after haematopoietic cell transplantation","volume":"59","author":"Fukushima","year":"2024","journal-title":"Bone Marrow Transplant."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"924","DOI":"10.1016\/S1470-2045(19)30167-6","article-title":"Atezolizumab in combination with carboplatin plus nab-paclitaxel chemotherapy compared with chemotherapy alone as first-line treatment for metastatic non-squamous non-small-cell lung cancer (IMpower130): A multicentre, randomised, open-label, phase 3 trial","volume":"20","author":"West","year":"2019","journal-title":"Lancet Oncol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1411","DOI":"10.1001\/jamaoncol.2019.2187","article-title":"Five-Year Survival and Correlates among Patients with Advanced Melanoma, Renal Cell Carcinoma, or Non-Small Cell Lung Cancer Treated with Nivolumab","volume":"5","author":"Topalian","year":"2019","journal-title":"JAMA Oncol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1056\/NEJMoa1801005","article-title":"Pembrolizumab plus Chemotherapy in Metastatic Non\u2013Small-Cell Lung Cancer","volume":"378","author":"Gandhi","year":"2018","journal-title":"N. Engl. J. Med."},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Boyero, L., S\u00e1nchez-Gastaldo, A., Alonso, M., Noguera-Ucl\u00e9s, J.F., Molina-Pinelo, S., and Bernab\u00e9-Caro, R. (2020). Primary and Acquired Resistance to Immunotherapy in Lung Cancer: Unveiling the Mechanisms Underlying of Immune Checkpoint Blockade Therapy. Cancers, 12.","DOI":"10.3390\/cancers12123729"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1186\/s12967-022-03409-4","article-title":"Transcriptomic datasets of cancer patients treated with immune-checkpoint inhibitors: A systematic review","volume":"20","year":"2022","journal-title":"J. Transl. Med."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Vu, S.H., Vetrivel, P., Kim, J., and Lee, M.-S. (2022). Cancer Resistance to Immunotherapy: Molecular Mechanisms and Tackling Strategies. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms231810906"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2315631","DOI":"10.1080\/19490976.2024.2315631","article-title":"The biotherapeutic Clostridium butyricum MIYAIRI 588 strain potentiates enterotropism of Ror\u03b3t+Treg and PD-1 blockade efficacy","volume":"16","author":"Oka","year":"2024","journal-title":"Gut Microbes"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"e258163","DOI":"10.1136\/bcr-2023-258163","article-title":"Management of a pregnant woman with a large cervical polyp and moderate genital bleeding in the first trimester","volume":"17","author":"Saitsu","year":"2024","journal-title":"BMJ Case Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.cmi.2015.10.014","article-title":"Clostridium butyricum: From beneficial to a new emerging pathogen","volume":"22","author":"Cassir","year":"2016","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2172666","DOI":"10.1080\/19490976.2023.2172666","article-title":"Neonatal necrotizing enterocolitis: Clostridium butyricum and Clostridium neonatale fermentation metabolism and enteropathogenicity","volume":"15","author":"Ferraris","year":"2023","journal-title":"Gut Microbes"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"17","DOI":"10.3109\/15569549909036015","article-title":"Structure and Function of Clostridium Botulinum Progenitor Toxin","volume":"18","author":"Oguma","year":"1999","journal-title":"J. Toxicol. Toxin Rev."},{"key":"ref_62","first-page":"21","article-title":"Assembly and Function of the Botulinum Neurotoxin Progenitor Complex","volume":"364","author":"Gu","year":"2013","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Smith, T.J., Hill, K.K., Foley, B.T., Detter, J.C., Munk, A.C., Bruce, D.C., Doggett, N.A., Smith, L.A., Marks, J.D., and Xie, G. (2007). Analysis of the Neurotoxin Complex Genes in Clostridium botulinum A1-A4 and B1 Strains: BoNT\/A3, \/Ba4 and \/B1 Clusters Are Located within Plasmids. PLoS ONE, 2.","DOI":"10.1371\/journal.pone.0001271"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"213","DOI":"10.4161\/mge.1.3.17617","article-title":"Horizontal gene transfer of toxin genes in Clostridium botulinum","volume":"1","author":"Skarin","year":"2011","journal-title":"Mob. Genet. Elem."},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Nawrocki, E.M., Bradshaw, M., and Johnson, E.A. (2018). Botulinum neurotoxin-encoding plasmids can be conjugatively transferred to diverse clostridial strains. Sci. Rep., 8.","DOI":"10.1038\/s41598-018-21342-9"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.ygeno.2013.12.003","article-title":"Comparison of assembled Clostridium botulinum A1 genomes revealed their evolutionary relationship","volume":"103","author":"Ng","year":"2014","journal-title":"Genomics"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Hill, K.K., Xie, G., Foley, B.T., Smith, T.J., Munk, A.C., Bruce, D., Smith, L.A., Brettin, T.S., and Detter, J.C. (2009). Recombination and insertion events involving the botulinum neurotoxin complex genes in Clostridium botulinum types A, B, E and F and Clostridium butyricum type E strains. BMC Biol., 7, Available online: https:\/\/bmcbiol.biomedcentral.com\/articles\/10.1186\/1741-7007-7-66.","DOI":"10.1186\/1741-7007-7-66"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"2963","DOI":"10.1128\/AEM.02623-06","article-title":"Flagellin Diversity in Clostridium botulinum Groups I and II: A New Strategy for Strain Identification","volume":"73","author":"Paul","year":"2007","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"3926","DOI":"10.1128\/AEM.00686-13","article-title":"Genetic Diversity of the Flagellin Genes of Clostridium botulinum Groups I and II","volume":"79","author":"Woudstra","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Valdezate, S., Carrasco, G., Medina, M.J., Garrido, N., Del Pino, S., Valiente, M., Pallar\u00e9s, M.P., and Villalon, P. (2023). Exploring the genetic background of the botulism neurotoxin BoNT\/B2 in Spain. Microbiol. Spectr., 11.","DOI":"10.1128\/spectrum.02380-23"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Smith, T.J., Tian, R., Imanian, B., Williamson, C.H.D., Johnson, S.L., Daligault, H.E., and Schill, K.M. (2021). Integration of Complete Plasmids Containing Bont Genes into Chromosomes of Clostridium parabotulinum, Clostridium sporogenes, and Clostridium argentinense. Toxins, 13.","DOI":"10.3390\/toxins13070473"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1007\/s00253-021-11741-w","article-title":"Botulinum toxin in cancer therapy\u2014Current perspectives and limitations","volume":"106","author":"Grenda","year":"2022","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.chom.2017.12.018","article-title":"Identification of a Botulinum Neurotoxin-like Toxin in a Commensal Strain of Enterococcus faecium","volume":"23","author":"Zhang","year":"2018","journal-title":"Cell Host Microbe"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Tehran, D.A., and Pirazzini, M. (2018). Novel Botulinum Neurotoxins: Exploring Underneath the Iceberg Tip. Toxins, 10.","DOI":"10.3390\/toxins10050190"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Poulain, B., and Popoff, M.R. (2019). Why Are Botulinum Neurotoxin-Producing Bacteria So Diverse and Botulinum Neurotoxins So Toxic?. Toxins, 11.","DOI":"10.3390\/toxins11010034"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Grenda, T., Jarosz, A., Sapa\u0142a, M., Stasiak, K., Grenda, A., Domaradzki, P., and Kwiatek, K. (2023). Molecular Diversity of BoNT-Producing Clostridia\u2014A Still-Emerging and Challenging Problem. Diversity, 15.","DOI":"10.3390\/d15030392"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1111\/j.1574-6968.2006.00171.x","article-title":"Diversity of the Clostridium coccoides group in human fecal microbiota as determined by 16S rRNA gene library","volume":"257","author":"Hayashi","year":"2006","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1099\/ijsem.0.000824","article-title":"Proposal to restrict the genus Clostridium Prazmowski to Clostridium butyricum and related species","volume":"66","author":"Lawson","year":"2016","journal-title":"Int. J. Syst. Evol. Microbiol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"e01469-18","DOI":"10.1128\/mBio.01469-18","article-title":"Botulinum Neurotoxin-Producing Bacteria. Isn\u2019t It Time that We Called a Species a Species?","volume":"9","author":"Smith","year":"2018","journal-title":"mBio"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/S0065-2911(09)05503-9","article-title":"Biology and Genomic Analysis of Clostridium botulinum","volume":"Volume 55","author":"Poole","year":"2009","journal-title":"Advances in Microbial Physiology"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"2191","DOI":"10.1128\/jcm.26.10.2191-2192.1988","article-title":"Genetic confirmation of identities of neurotoxigenic Clostridium baratii and Clostridium butyricum implicated as agents of infant botulism","volume":"26","author":"Suen","year":"1988","journal-title":"J. Clin. Microbiol."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/9\/780\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:53:17Z","timestamp":1760111597000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/13\/9\/780"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,10]]},"references-count":81,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2024,9]]}},"alternative-id":["pathogens13090780"],"URL":"https:\/\/doi.org\/10.3390\/pathogens13090780","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,10]]}}}