{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T23:39:27Z","timestamp":1790379567705,"version":"4.1.0"},"reference-count":63,"publisher":"Frontiers Media SA","content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"DOI":"10.3389\/fmicb.2017.00545","type":"journal-article","created":{"date-parts":[[2017,4,3]],"date-time":"2017-04-03T03:38:18Z","timestamp":1491190698000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":24,"title":["Genetic Characterization of the Exceptionally High Heat Resistance of the Non-toxic Surrogate Clostridium sporogenes PA 3679"],"prefix":"10.3389","volume":"8","author":[{"given":"Robert R.","family":"Butler","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristin M.","family":"Schill","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yun","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Fran\u00e7ois","family":"Pombert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2017,4,3]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"B2","doi-asserted-by":"crossref","first-page":"4563","DOI":"10.1016\/S0021-9258(18)99755-3","article-title":"Biosynthesis of dipicolinic acid in sporulating Bacillus megaterium","volume":"241","author":"Bach","year":"1966","journal-title":"J. Biol. Chem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"2633","DOI":"10.1038\/ismej.2016.59","article-title":"A mobile genetic element profoundly increases heat resistance of bacterial spores","volume":"10","author":"Berendsen","year":"2016","journal-title":"ISME J."},{"key":"B4","doi-asserted-by":"publisher","first-page":"779","DOI":"10.4315\/0362-028X.JFP-11-391","article-title":"Clostridium sporogenes PA 3679 and its uses in the derivation of thermal processing schedules for low-acid shelf-stable foods and as a research model for proteolytic Clostridium botulinum","volume":"75","author":"Brown","year":"2012","journal-title":"J. Food Prot."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1702","DOI":"10.3389\/fmicb.2016.01702","article-title":"Diversity of the germination apparatus in Clostridium botulinum groups I, II, III, and IV","volume":"7","author":"Brunt","year":"2016","journal-title":"Front. Microbiol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"434","DOI":"10.1128\/AEM.01426-08","article-title":"Synergistic inactivation of spores of proteolytic Clostridium botulinum strains by high pressure and heat is strain and product dependent","volume":"75","author":"Bull","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0378-1119(99)00124-9","article-title":"Regulation of four genes encoding small, acid-soluble spore proteins in Bacillus subtilis","volume":"232","author":"Cabrera-Hernandez","year":"1999","journal-title":"Gene"},{"key":"B8","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1111\/j.1574-6968.1991.tb04335.x","article-title":"Cloning and nucleotide sequence of three genes coding for small, acid-soluble proteins of Clostridium perfringens spores","volume":"61","author":"Cabrera-Martinez","year":"1991","journal-title":"FEMS Microbiol. Lett."},{"key":"B9","doi-asserted-by":"publisher","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":"B10","doi-asserted-by":"publisher","first-page":"210","DOI":"10.1186\/1471-2148-10-210","article-title":"BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments","volume":"10","author":"Criscuolo","year":"2010","journal-title":"BMC Evol. Biol."},{"key":"B11","first-page":"1","article-title":"The igraph software package for complex network research","volume":"1695","author":"Cs\u00e1rdi","year":"2006","journal-title":"Inter J. Complex Syst."},{"key":"B12","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1006\/jmbi.1993.1403","article-title":"Cloning, DNA sequence, functional analysis and transcriptional regulation of the genes encoding dipicolinic acid synthetase required for sporulation in Bacillus subtilis","volume":"232","author":"Daniel","year":"1993","journal-title":"J. Mol. Biol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1016\/j.ijfoodmicro.2013.12.029","article-title":"Meta-analysis of D-values of proteolytic Clostridium botulinum and its surrogate strain Clostridium sporogenes PA 3679","volume":"174","author":"Diao","year":"2014","journal-title":"Int. J. Food Microbiol."},{"key":"B14","first-page":"472","article-title":"Distribution of Clostridium botulinum in the environment and its significance in relation to botulism","volume-title":"Proceedings of the 5th International Symposium on Microbial Ecology","author":"Dodds","year":"1989"},{"key":"B15","doi-asserted-by":"publisher","first-page":"1694","DOI":"10.1128\/JB.00986-15","article-title":"Characterization of Clostridium difficile spores lacking either SpoVA or dipicolinic acid synthetase","volume":"198","author":"Donnelly","year":"2016","journal-title":"J. Bacteriol."},{"key":"B16","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1201\/9780203489819.ch29","article-title":"Sporulation in clostridia (Genetics)","volume-title":"Handbook on Clostridia","author":"D\u00fcrre","year":"2005"},{"key":"B17","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1016\/S0022-2836(03)00205-5","article-title":"The \u03c3E regulon and the identification of additional sporulation genes in Bacillus subtilis","volume":"327","author":"Eichenberger","year":"2003","journal-title":"J. Mol. Biol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1186\/s13059-015-0721-2","article-title":"OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy","volume":"16","author":"Emms","year":"2015","journal-title":"Genome Biol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"2870","DOI":"10.1111\/j.1462-2920.2012.02841.x","article-title":"Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes","volume":"14","author":"Galperin","year":"2012","journal-title":"Environ. Microbiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1128\/AEM.01965-10","article-title":"Effects of Mn and Fe levels on Bacillus subtilis spore resistance and effects of Mn2+, other divalent cations, orthophosphate, and dipicolinic acid on protein resistance to ionizing radiation","volume":"77","author":"Granger","year":"2011","journal-title":"Appl. Environ. Microbiol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1111\/j.1365-2621.1946.tb16368.x","article-title":"Bacteriological studies relating to thermal processing of canned meats. V. Characteristics of putrefactive anaerobe used in thermal resistance studies","volume":"11","author":"Gross","year":"1946","journal-title":"J. Food Sci."},{"key":"B22","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1093\/sysbio\/syq010","article-title":"New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0","volume":"59","author":"Guindon","year":"2010","journal-title":"Syst. Biol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1111\/j.1574-6968.2004.tb09487.x","article-title":"Disruption of the gene (spo0A) encoding sporulation transcription factor blocks endospore formation and enterotoxin production in enterotoxigenic Clostridium perfringens type A","volume":"233","author":"Huang","year":"2004","journal-title":"FEMS Microbiol. Lett."},{"key":"B24","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1111\/j.1365-2672.1951.tb01995.x","article-title":"A discussion of the literature on botulism in relation to acid foods","volume":"14","author":"Ingram","year":"1951","journal-title":"Proc. Soc. Appl. Bacteriol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1236","DOI":"10.1093\/bioinformatics\/btu031","article-title":"InterProScan 5: genome-scale protein function classification","volume":"30","author":"Jones","year":"2014","journal-title":"Bioinformatics"},{"key":"B26","doi-asserted-by":"publisher","first-page":"1511","DOI":"10.1038\/nprot.2012.085","article-title":"Template-based protein structure modeling using the RaptorX web server","volume":"7","author":"K\u00e4llberg","year":"2012","journal-title":"Nat. Protoc."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1647","DOI":"10.1093\/bioinformatics\/bts199","article-title":"Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data","volume":"28","author":"Kearse","year":"2012","journal-title":"Bioinformatics"},{"key":"B28","doi-asserted-by":"publisher","first-page":"6954","DOI":"10.1128\/AEM.02134-14","article-title":"Genetic characterization and comparison of Clostridium botulinum isolates from botulism cases in Japan between 2006 and 2011","volume":"80","author":"Kenri","year":"2014","journal-title":"Appl. Environ. Microbiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"2806","DOI":"10.1073\/pnas.0708244105","article-title":"Structure of a protein-DNA complex essential for DNA protection in spores of Bacillus species","volume":"105","author":"Lee","year":"2008","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B30","doi-asserted-by":"publisher","first-page":"e1000056","DOI":"10.1371\/journal.ppat.1000056","article-title":"A novel small acid soluble protein variant is important for spore resistance of most Clostridium perfringens food poisoning isolates","volume":"4","author":"Li","year":"2008","journal-title":"PLoS Pathog."},{"key":"B31","doi-asserted-by":"publisher","first-page":"e6249","DOI":"10.1371\/journal.pone.0006249","article-title":"Further characterization of Clostridium perfringens small acid soluble protein-4 (Ssp4) properties and expression","volume":"4","author":"Li","year":"2009","journal-title":"PLoS ONE"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1875","DOI":"10.1128\/JB.00062-12","article-title":"Role of a SpoVA protein in dipicolinic acid uptake into developing spores of Bacillus subtilis","volume":"194","author":"Li","year":"2012","journal-title":"J. Bacteriol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1093\/infdis\/60.1.122","article-title":"Studies on anaerobic bacteria X. heat stable and heat labile antigens in the botulinus and related groups of sporebearing anaerobes","volume":"60","author":"McClung","year":"1937","journal-title":"J. Infect. Dis."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1683","DOI":"10.1046\/j.1365-2958.2003.03818.x","article-title":"The Spo0A regulon of Bacillus subtilis","volume":"50","author":"Molle","year":"2003","journal-title":"Mol. Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1099\/00221287-100-2-395","article-title":"Clostridium sporogenes isolates and their relationship to C. botulinum based on deoxyribonucleic acid reassociation","volume":"100","author":"Nakamura","year":"1977","journal-title":"J. Gen. Microbiol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"132","DOI":"10.1186\/s13059-016-0997-x","article-title":"Mash: fast genome and metagenome distance estimation using MinHash","volume":"17","author":"Ondov","year":"2016","journal-title":"Genome Biol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1007\/s00203-004-0696-y","article-title":"Sporulation genes in members of the low G+C Gram-type-positive phylogenetic branch (Firmicutes)","volume":"182","author":"Onyenwoke","year":"2004","journal-title":"Arch. Microbiol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"178","DOI":"10.1111\/j.1365-2958.2009.06975.x","article-title":"EtfA catalyses the formation of dipicolinic acid in Clostridium perfringens","volume":"75","author":"Orsburn","year":"2010","journal-title":"Mol. Microbiol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"188","DOI":"10.1111\/j.1574-6968.2008.01454.x","article-title":"The SpmA\/B and DacF proteins of Clostridium perfringens play important roles in spore heat resistance","volume":"291","author":"Orsburn","year":"2009","journal-title":"FEMS Microbiol. Lett."},{"key":"B40","doi-asserted-by":"publisher","first-page":"3691","DOI":"10.1093\/bioinformatics\/btv421","article-title":"Roary: rapid large-scale prokaryote pan genome analysis","volume":"31","author":"Page","year":"2015","journal-title":"Bioinformatics"},{"key":"B41","doi-asserted-by":"publisher","first-page":"5505","DOI":"10.1128\/JB.182.19.5505-5512.2000","article-title":"Characterization of spores of Bacillus subtilis which lack dipicolinic acid","volume":"182","author":"Paidhungat","year":"2000","journal-title":"J. Bacteriol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"3730","DOI":"10.1128\/AEM.00169-08","article-title":"Roles of DacB and Spm proteins in Clostridium perfringens spore resistance to moist heat, chemicals, and UV radiation","volume":"74","author":"Paredes-Sabja","year":"2008a","journal-title":"Appl. Environ. Microbiol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"4648","DOI":"10.1128\/JB.00325-08","article-title":"Characterization of Clostridium perfringens spores that lack SpoVA proteins and dipicolinic acid","volume":"190","author":"Paredes-Sabja","year":"2008b","journal-title":"J. Bacteriol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"2077","DOI":"10.1128\/JB.01546-14","article-title":"Function of the SpoVAEa and SpoVAF proteins of Bacillus subtilis spores","volume":"196","author":"Perez-Valdespino","year":"2014","journal-title":"J. Bacteriol."},{"key":"B45","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1128\/JB.181.1.126-132.1999","article-title":"Roles of low-molecular-weight penicillin-binding proteins in Bacillus subtilis spore peptidoglycan synthesis and spore properties","volume":"181","author":"Popham","year":"1999","journal-title":"J. Bacteriol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"2315","DOI":"10.1128\/JB.185.7.2315-2329.2003","article-title":"Identification of a new gene essential for germination of Bacillus subtilis spores with Ca2+-dipicolinate","volume":"185","author":"Ragkousi","year":"2003","journal-title":"J. Bacteriol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"50","DOI":"10.1186\/1471-2180-6-50","article-title":"Investigating the role of small, acid-soluble spore proteins (SASPs) in the resistance of Clostridium perfringens spores to heat","volume":"6","author":"Raju","year":"2006","journal-title":"BMC Microbiol."},{"key":"B48","volume-title":"R: A Language and Environment for Statistical Computing","author":"R Core Team T","year":"2016"},{"key":"B49","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1038\/nrmicro3295","article-title":"Botulinum neurotoxins: genetic, structural and mechanistic insights","volume":"12","author":"Rossetto","year":"2014","journal-title":"Nat. Rev. Microbiol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1128\/AEM.02616-15","article-title":"Genetic diversity of Clostridium sporogenes PA 3679 isolates obtained from different sources as resolved by pulsed-field gel electrophoresis and high-throughput sequencing","volume":"82","author":"Schill","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"514","DOI":"10.1111\/j.1365-2672.2005.02736.x","article-title":"Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals","volume":"101","author":"Setlow","year":"2006","journal-title":"J. Appl. Microbiol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1016\/j.tim.2007.02.004","article-title":"I will survive: DNA protection in bacterial spores","volume":"15","author":"Setlow","year":"2007","journal-title":"Trends Microbiol."},{"key":"B53","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1128\/JB.01455-13","article-title":"Germination of spores of Bacillus Species: what we know and do not know","volume":"196","author":"Setlow","year":"2014a","journal-title":"J. Bacteriol."},{"key":"B54","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1128\/microbiolspec.TBS-0003-2012","article-title":"Spore Resistance Properties","volume":"2","author":"Setlow","year":"2014b","journal-title":"Microbiol. Spectr."},{"key":"B55","doi-asserted-by":"publisher","first-page":"1316","DOI":"10.1111\/j.1365-2621.1975.tb01080.x","article-title":"Thermal process lethality guide for low-acid foods in metal containers","volume":"40","author":"Stumbo","year":"1975","journal-title":"J. Food Sci."},{"key":"B56","doi-asserted-by":"publisher","first-page":"1009","DOI":"10.1093\/bioinformatics\/btr039","article-title":"Easyfig: a genome comparison visualizer","volume":"27","author":"Sullivan","year":"2011","journal-title":"Bioinformatics"},{"key":"B57","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1128\/JB.184.2.584-587.2002","article-title":"The products of the spoVA operon are involved in dipicolinic acid uptake into developing spores of Bacillus subtilis","volume":"184","author":"Tovar-Rojo","year":"2002","journal-title":"J. Bacteriol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1111\/j.1365-2621.1938.tb17065.x","article-title":"Heat-resistance studies on spores of putrefactive anaerobes in relation to determination of safe processes for canned foods","volume":"3","author":"Townsend","year":"1938","journal-title":"J. Food Sci."},{"key":"B59","doi-asserted-by":"publisher","first-page":"813","DOI":"10.1111\/mmi.12591","article-title":"Bacillus subtilis spore protein SpoVAC functions as a mechanosensitive channel","volume":"92","author":"Vel\u00e1squez","year":"2014","journal-title":"Mol. Microbiol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.jmb.2006.01.059","article-title":"The forespore line of gene expression in Bacillus subtilis","volume":"358","author":"Wang","year":"2006","journal-title":"J. Mol. Biol."},{"key":"B61","doi-asserted-by":"publisher","first-page":"5420","DOI":"10.1128\/AEM.01159-15","article-title":"Implications of genome-based discrimination between Clostridium botulinum group I and Clostridium sporogenes strains for bacterial taxonomy","volume":"81","author":"Weigand","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"2098","DOI":"10.1099\/mic.0.000162","article-title":"Small acid-soluble spore proteins of Clostridium acetobutylicum are able to protect DNA in vitro and are specifically cleaved by germination protease GPR and spore protease YyaC","volume":"161","author":"Wetzel","year":"2015","journal-title":"Microbiology"},{"key":"B63","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1186\/s12864-016-2502-z","article-title":"Comparative genomic analyses reveal broad diversity in botulinum-toxin-producing Clostridia","volume":"17","author":"Williamson","year":"2016","journal-title":"BMC Genomics"}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"http:\/\/journal.frontiersin.org\/article\/10.3389\/fmicb.2017.00545\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,27]],"date-time":"2022-07-27T04:12:37Z","timestamp":1658895157000},"score":1,"resource":{"primary":{"URL":"http:\/\/journal.frontiersin.org\/article\/10.3389\/fmicb.2017.00545\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,4,3]]},"references-count":63,"URL":"https:\/\/doi.org\/10.3389\/fmicb.2017.00545","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,4,3]]}}}