Implications of genome-based discrimination between Clostridium botulinum group I and Clostridium sporogenes strains for bacterial taxonomy

Applied and Environmental Microbiology

Volumn 81, Issue 16, 2015, Pages 5420-5429

  Weigand, Michael R ^a   Pena Gonzalez, Angela ^b   Shirey, Timothy B ^c   Broeker, Robin G ^c   Ishaq, Maliha K ^c   Konstantinidis, Konstantinos T ^a,b   Raphael, Brian H ^c  

^a Georgia Institute of Technology   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM; GENE TRANSFER; GENES;

BACTERIAL TAXONOMIES; BOTULINUM NEUROTOXINS; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM SPOROGENES; HORIZONTAL GENE TRANSFER; MOLECULAR IDENTIFICATION; PHYLOGENETIC RECONSTRUCTION; PHYLOGENETIC RELATIONSHIPS;

BACTERIA;

BACTERIUM; BIOASSAY; CLADISTICS; CLASSIFICATION; GENE FLOW; GENE TRANSFER; GENOME; IDENTIFICATION KEY; MOLECULAR ANALYSIS; PHYLOGENETICS; TAXONOMY;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM SPOROGENES;

BACTERIAL DNA;

BACTERIAL GENOME; CHEMISTRY; CHROMOSOME; CLASSIFICATION; CLOSTRIDIUM; CLUSTER ANALYSIS; DNA SEQUENCE; GENE LOCUS; GENETICS; GENOTYPE; MOLECULAR GENETICS; PHYLOGENY; PLASMID; SEQUENCE HOMOLOGY;

CHROMOSOMES; CLOSTRIDIUM; CLUSTER ANALYSIS; DNA, BACTERIAL; GENETIC LOCI; GENOME, BACTERIAL; GENOTYPE; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

EID: 84937846883     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01159-15     Document Type: Article

References (50)

1. Brown JL, Tran-Dinh N, Chapman B. 2012. 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. J Food Prot 75:779-792. http://dx.doi.org/10.4315/0362-028X.JFP-11-391.
2. Cato EP, Hash DE, Holdeman LV, Moore WEC. 1982. Electrophoretic study of Clostridium species. J Clin Microbiol 15:688-702.
3. Farshy DC, Moss CW. 1970. Characterization of clostridia by gas chromatography:differentiation of species by trimethylsilyl dervatives of whole-cell hydrolysates. Appl Environ Microbiol 20:78-84.
4. Lee WH, Riemann H. 1970. The genetic relatedness of proteolytic Clostridium botulinum strains. J Gen Microbiol 64:85-90. http://dx.doi.org/10.1099/00221287-64-1-85.
5. Nakamura S, Okado I, Nakashio S, Nishida S. 1977. Clostridium sporogenes isolates and their relationships to C. botulinum on deoxyribonucleic acid reassociation. J Gen Microbiol 100:395-401. http://dx.doi.org/10.1099/00221287-100-2-395.
6. Hutson RA, Thompson DE, Lawson PA, Schocken-Itturino RP, Böttger EC, Collins MD. 1993. Genetic interrelationships of proteolytic Clostridium botulinum types A, B, and F and other members of the Clostridium botulinum complex as revealed by small-subunit rRNA gene sequences. Antonie Van Leeuwenhoek 64:273-283.
7. Kalia VC, Mukherjee T, Bhushan A, Joshi J, Shankar P, Huma N. 2011. Analysis of the unexplored features of rrs (16S rDNA) of the genus Clostridium (2011). BMC Genomics 12:18. http://dx.doi.org/10.1186/1471-2164-12-18.
8. Olsen I, Johnson JL, Moore LVH, Moore WEC. 1995. Rejection of Clostridium putrificum and conservation of Clostridium botulinum and Clostridium sporogenes. Int J Syst Bacteriol 45:414. http://dx.doi.org/10.1099/00207713-45-2-414.
9. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP. 2009. The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741-746. http://dx.doi.org/10.1126/science.1159388.
10. Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J. 2005. Opinion: re-evaluating prokaryotic species. Nat Rev Microbiol 3:733-739. http://dx.doi.org/10.1038/nrmicro1236.
11. Konstantinidis KT, Tiedje JM. 2005. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 102:2567-2572. http://dx.doi.org/10.1073/pnas.0409727102.
12. Konstantinidis KT, Ramette A, Tiedje JM. 2006. The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 361:1929-1940. http://dx.doi.org/10.1098/rstb.2006.1920.
13. Lawrence JG. 2002. Gene transfer in bacteria: speciation without species?. Theor Popul Biol 61:449-460. http://dx.doi.org/10.1006/tpbi.2002.1587.
14. Maslanka SE, Solomon HM, Sharma S, Johnson EA. 2013. Clostridium botulinum and its toxins. In Doores S, Salfinger Y, Tortorello ML, Wilcke BW (ed), Compendium of methods for the microbiological examination of foods, 5th ed. American Public Health Association, Washington, DC.
15. Maslanka SE, Lúquez C, Raphael BH, Dykes JK, Joseph LA. 2011. Utility of botulinum toxin ELISA A, B, E, F kits for clinical laboratory investigations of human botulism. Botulinum J 2:72-92. http://dx.doi.org/10.1504/TBJ.2011.041817.
16. Raphael BH, Choudoir MJ, Lúquez C, Fernández R, Maslanka SE. 2010. Sequence diversity of genes encoding botulinum neurotoxin type F. Appl Environ Microbiol 76:4805-4812. http://dx.doi.org/10.1128/AEM.03109-09.
17. Cox MP, Peterson DA, Biggs PJ. 2010. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485. http://dx.doi.org/10.1186/1471-2105-11-485.
18. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821-829. http://dx.doi .org/10.1101/gr.074492.107.
19. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaogian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J. 2012. SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience 1:18. http://dx.doi.org/10.1186/2047-217X-1-18.
20. Luo C, Tsementzi D, Kyrpides NC, Konstantinidis KT. 2012. Individual genome assembly from complex community short-read metagenomic datasets. ISME J 6:898-901. http://dx.doi.org/10.1038/ismej.2011.147.
21. Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT. 2009. Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 25:2071-2073. http://dx.doi.org/10.1093/bioinformatics/btp356.
22. Darling AE, Tritt A, Eisen JA, Facciotti MT. 2011. Mauve assembly metrics. Bioinformatics 27:2756-2757. http://dx.doi.org/10.1093/bioinformatics /btr451.
23. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. http://dx.doi.org/10.1186/1471-2164-9-75.
24. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. 2011. BLAST ring image generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402. http://dx.doi.org/10.1186/1471-2164-12-402.
25. Guy L, Kultima JR, Andersson SG. 2010. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 26:2334-2335. http://dx .doi.org/10.1093/bioinformatics/btq413.
26. Besemer J, Lomsadze A, Borodovsky M. 2001. GeneMarkS: a selftraining method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29:2607-2618.
27. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM, Konstantinidis KT. 2011. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci U S A 108:7200-7205. http://dx.doi.org/10.1073/pnas.1015622108.
28. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. http://dx.doi .org/10.1093/nar/gkh340.
29. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254-267.
30. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
31. de Hoon MJ, Imoto S, Nolan J, Miyano S. 2004. Open source clustering software. Bioinformatics 20:1453-1454. http://dx.doi.org /10.1093/bioinformatics/bth078.
32. UniProt Consortium. 2014. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 42:D191-D198. http://dx.doi.org/10.1093/nar/gkt1140.
33. Boratyn GM, Schaffer AA, Agarwala R, Altschul SF, Lipman DJ, Madden TL. 2012. Domain enhanced lookup time accelerated BLAST. Biol Direct 7:2. http://dx.doi.org/10.1186/1745-6150-7-2.
34. Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Marchler GH, Mullokandov M, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Yamashita RA, Yin JJ, Zhang D, Bryant SH. 2005. CDD: a conserved domain database for protein classification. Nucleic Acids Res 33:D192-D196.
35. Hill KK, Smith TJ, Helma CH, Ticknor LO, Foley BT, Svensson RT, Brown JL, Johnson EA, Smith LA, Okinaka RT, Jackson PJ, Marks JD. 2007. Genetic diversity among botulinum neurotoxin-producing clostridial strains. J Bacteriol 189:818-832. http://dx.doi.org/10.1128/JB.01180-06.
36. Hill KK, Xie G, Foley BT, Smith TJ, Munk AC, Bruce D, Smith LA, Brettin TS, Detter JC. 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 7:66. http://dx.doi.org/10.1186/1741-7007-7-66.
37. Bradbury M, Greenfield P, Midgley D, Li D, Tran-Dinh N, Vriesekoop F, Brown JL. 2012. Draft genome sequence of Clostridium sporogenes PA 3679, the common nontoxigenic surrogate for proteolytic Clostridium botulinum. J Bacteriol 194:1631-1632. http://dx.doi.org/10.1128/JB.06765-11.
38. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. 2007. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81-91. http://dx.doi.org/10.1099/ijs.0.64483-0.
39. Ionata E, Canganella F, Bianconi G, Benno Y, Sakamoto M, Capasso A, Rossi M, La Cara F. 2008. A novel keratinase from Clostridium sporogenes bv. pennavorans bv. nov., a thermotolerant organism isolated from solfataric muds. Microbiol Res 163:105-112. http://dx.doi.org/10.1016/j.micres.2006.08.001.
40. Raphael BH, Bradshaw M, Kalb SR, Joseph LA, Lúquez C, Barr JR, Johnson EA, Maslanka SE. 2014. Clostridium botulinum strains producing BoNT/F4 or BoNT/F5. Appl Environ Microbiol 80:3250-3257. http://dx.doi.org/10.1128/AEM.00284-14.
41. McClung LS. 1937. Studies on anerobic bacteria. X. Heat stable and heat liable antigens in the botulinus and related groups of spore-bearing anaerobes. J Infect Dis 60:122-128.
42. Townsend CT, Esty JR, Baselt FC. 1938. Heat-resistance studies on spores of putrefactive anaerobes in relation to determination of safe processes for canned foods. J Food Sci 3:323-346. http://dx.doi.org/10.1111/j .1365-2621.1938.tb17065.x.
43. Kenri T, Sekizuka T, Yamamoto A, Iwaki M, Komiya T, Hatakeyama T, Nakajima H, Takahashi M, Kuroda M, Shibayama K. 2014. Genetic characterization and comparison of Clostridium botulinum isolates from botulism cases in Japan between 2006 and 2011. Appl Environ Microbiol 80:6954-6964. http://dx.doi.org/10.1128/AEM.02134-14.
44. Carter AT, Paul CJ, Mason DR, Twine SM, Alston MJ, Logan SM, Austin JW, Peck MW. 2009. Independent evolution of neurotoxin and flagellar genetic loci in proteolyticClostridium botulinum. BMCGenomics 10:115. http://dx.doi.org/10.1186/1471-2164-10-115.
45. Franciosa G, Maugliani A, Scalfaro C, Aureli P. 2009. Evidence that plasmid-borne botulinum neurotoxin type B genes are widespread among Clostridium botulinum serotype B strains. PLoS One 4:e4829. http://dx .doi.org/10.1371/journal.pone.0004829.
46. Marshall KM, Bradshaw M, Johnson EA. 2010. Conjugative botulinum neurotoxin-encoding plasmids in Clostridium botulinum. PLoS One 11:e11087. http://dx.doi.org/10.1371/journal.pone.0011087.
47. Umeda K, Seto Y, Kohda T, Mukamoto M, Kozaki S. 2012. Stability of toxigenicity in proteolytic Clostridium botulinum type B upon serial passage. Microbiol Immunol 56:338-341. http://dx.doi.org/10.1111/j.1348-0421.2012.00441.x.
48. Marshall KM, Bradshaw M, Pellett S, Johnson EA. 2007. Plasmid encoded neurotoxin genes in Clostridium botulinum serotype A subtypes. Biochem Biophys Res Commun 14:49-54.
49. Smith TJ, Hill KK, Xie G, Foley BT, Williamson CH, Foster JT, Johnson SL, Chertkov O, Teshima H, Gibbons HS, Johnsky LA, Karavis MA, Smith LA. 2015. Genomic sequences of six botulinum neurotoxinproducing strains representing three clostridial species illustrate the mobility and diversity of botulinum neurotoxin genes. Infect Genet Evol 30:102-113. http://dx.doi.org/10.1016/j.meegid.2014.12.002.
50. Fillo S, Giordani F, Anselmo A, Fortunato A, Palozzi AM, De Santis R, Ciammaruconi A, Spagnolo F, Anniballi F, Fiore A, Auricchio B, De Medici D, Lista F. 2015. Draft genome sequence of Clostridium botulinum B2 450 strain from wound botulism in a drug user in Italy. Genome Announc 3:e00238-15. http://dx.doi.org/10.1128/genomeA.00238-15.