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The Phylogeny of the Genus Clostridium: Proposal of Five New Genera and Eleven New Species Combinations

¹Institute of Food Research, Department of Microbiology, Earley Gate, Reading RG6 2EF, United Kingdom
²Deutsche Sammlung von Mikroorganismen und Zellkulturen, D-38124 Braunschweig, Germany

^* Corresponding author. Mailing address: Institute of Food Research, Reading Laboratory, Earley Gate, Whiteknights Road, Reading RG6 2EF, United Kingdom. Phone: (0734) 357226. Fax: (0734) 267917.

ABSTRACT

The 16S rRNA gene sequences of 34 named and unnamed clostridial strains were determined by PCR direct sequencing and were compared with more than 80 previously determined clostridial sequences and the previously published sequences of representative species of other low- G+C-content gram-positive genera, thereby providing an almost complete picture of the genealogical interrelationships of the clostridia. The results of our phylogenetic analysis corroborate and extend previous findings in showing that the genus Clostridium is extremely heterogeneous, with many species phylogenetically intermixed with other sporeforming and non-sporeforming genera. The genus Clostridium is clearly in need of major revision, and the rRNA structures defined in this and previous studies may provide a sound basis for future taxonomic restructuring. The problems and different possibilities for restructuring are discussed in light of the phenotypic and phylogenetic data, and a possible hierarchical structure for the clostridia and their close relatives is presented. On the basis of phenotypic criteria and the results of phylogenetic analyses the following five new genera and 11 new combinations are proposed: Caloramator gen. nov., with Caloramator fervidus comb. nov.; Filifactor gen. nov., with Filifactor villosus comb. nov.; Moorella gen. nov., with Moorella thermoacetica comb. nov. and Moorella thermoautotrophica comb. nov.; Oxobacter gen. nov., with Oxobacter pfennigii comb. nov.; Oxalophagus gen. nov., with Oxalophagus oxalicus comb. nov.; Eubacterium barkeri comb. nov.; Paenibacillus durum comb. nov.; Thermoanaerobacter kivui comb. nov.; Thermoanaerobacter thermocopriae comb. nov.; and Thermoanerobacterium thermosaccharolyticum comb. nov.

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				S. M. Finegold, D. Molitoris, M.-L. Vaisanen, Y. Song, C. Liu, and M. Bolanos In Vitro Activities of OPT-80 and Comparator Drugs against Intestinal Bacteria Antimicrob. Agents Chemother., December 1, 2004; 48(12): 4898 - 4902. [Abstract] [Full Text] [PDF]

				T. Matsuki, K. Watanabe, J. Fujimoto, T. Takada, and R. Tanaka Use of 16S rRNA Gene-Targeted Group-Specific Primers for Real-Time PCR Analysis of Predominant Bacteria in Human Feces Appl. Envir. Microbiol., December 1, 2004; 70(12): 7220 - 7228. [Abstract] [Full Text] [PDF]

				L. Lemee, A. Dhalluin, S. Testelin, M.-A. Mattrat, K. Maillard, J.-F. Lemeland, and J.-L. Pons Multiplex PCR Targeting tpi (Triose Phosphate Isomerase), tcdA (Toxin A), and tcdB (Toxin B) Genes for Toxigenic Culture of Clostridium difficile J. Clin. Microbiol., December 1, 2004; 42(12): 5710 - 5714. [Abstract] [Full Text] [PDF]

				P. C. Y. Woo, S. K. P. Lau, G. K. S. Woo, A. M. Y. Fung, V. P. Y. Yiu, and K.-y. Yuen Bacteremia Due to Clostridium hathewayi in a Patient with Acute Appendicitis J. Clin. Microbiol., December 1, 2004; 42(12): 5947 - 5949. [Abstract] [Full Text] [PDF]

				S. Kato, S. Haruta, Z. J. Cui, M. Ishii, A. Yokota, and Y. Igarashi Clostridium straminisolvens sp. nov., a moderately thermophilic, aerotolerant and cellulolytic bacterium isolated from a cellulose-degrading bacterial community Int J Syst Evol Microbiol, November 1, 2004; 54(6): 2043 - 2047. [Abstract] [Full Text] [PDF]

				S. Chen and X. Dong Acetanaerobacterium elongatum gen. nov., sp. nov., from paper mill waste water Int J Syst Evol Microbiol, November 1, 2004; 54(6): 2257 - 2262. [Abstract] [Full Text] [PDF]

				Y. Song, C. Liu, and S. M. Finegold Real-Time PCR Quantitation of Clostridia in Feces of Autistic Children Appl. Envir. Microbiol., November 1, 2004; 70(11): 6459 - 6465. [Abstract] [Full Text] [PDF]

				T. Miyamoto, M. Kawahara, and K. Minamisawa Novel Endophytic Nitrogen-Fixing Clostridia from the Grass Miscanthus sinensis as Revealed by Terminal Restriction Fragment Length Polymorphism Analysis Appl. Envir. Microbiol., November 1, 2004; 70(11): 6580 - 6586. [Abstract] [Full Text] [PDF]

				H. Jeong, H. Yi, Y. Sekiguchi, M. Muramatsu, Y. Kamagata, and J. Chun Clostridium jejuense sp. nov., isolated from soil Int J Syst Evol Microbiol, September 1, 2004; 54(5): 1465 - 1468. [Abstract] [Full Text] [PDF]

				J.-W. Bae, J. R. Park, Y.-H. Chang, S.-K. Rhee, B.-C. Kim, and Y.-H. Park Clostridium hastiforme is a later synonym of Tissierella praeacuta Int J Syst Evol Microbiol, May 1, 2004; 54(3): 947 - 949. [Abstract] [Full Text] [PDF]

				K. Minamisawa, K. Nishioka, T. Miyaki, B. Ye, T. Miyamoto, M. You, A. Saito, M. Saito, W. L. Barraquio, N. Teaumroong, et al. Anaerobic Nitrogen-Fixing Consortia Consisting of Clostridia Isolated from Gramineous Plants Appl. Envir. Microbiol., May 1, 2004; 70(5): 3096 - 3102. [Abstract] [Full Text] [PDF]

				P. C. Burrell, C. O'Sullivan, H. Song, W. P. Clarke, and L. L. Blackall Identification, Detection, and Spatial Resolution of Clostridium Populations Responsible for Cellulose Degradation in a Methanogenic Landfill Leachate Bioreactor Appl. Envir. Microbiol., April 1, 2004; 70(4): 2414 - 2419. [Abstract] [Full Text] [PDF]

				P. Louis, S. H. Duncan, S. I. McCrae, J. Millar, M. S. Jackson, and H. J. Flint Restricted Distribution of the Butyrate Kinase Pathway among Butyrate-Producing Bacteria from the Human Colon J. Bacteriol., April 1, 2004; 186(7): 2099 - 2106. [Abstract] [Full Text] [PDF]

				P. A. Lawson, Y. Song, C. Liu, D. R. Molitoris, M.-L. Vaisanen, M. D. Collins, and S. M. Finegold Anaerotruncus colihominis gen. nov., sp. nov., from human faeces Int J Syst Evol Microbiol, March 1, 2004; 54(2): 413 - 417. [Abstract] [Full Text] [PDF]

				L. Urios, V. Cueff, P. Pignet, and G. Barbier Tepidibacter formicigenes sp. nov., a novel spore-forming bacterium isolated from a Mid-Atlantic Ridge hydrothermal vent Int J Syst Evol Microbiol, March 1, 2004; 54(2): 439 - 443. [Abstract] [Full Text] [PDF]

				S. Verbarg, H. Rheims, S. Emus, A. Fruhling, R. M. Kroppenstedt, E. Stackebrandt, and P. Schumann Erysipelothrix inopinata sp. nov., isolated in the course of sterile filtration of vegetable peptone broth, and description of Erysipelotrichaceae fam. nov. Int J Syst Evol Microbiol, January 1, 2004; 54(1): 221 - 225. [Abstract] [Full Text] [PDF]

				T. R. Whitehead, M. A. Cotta, M. D. Collins, and P. A. Lawson Hespellia stercorisuis gen. nov., sp. nov. and Hespellia porcina sp. nov., isolated from swine manure storage pits Int J Syst Evol Microbiol, January 1, 2004; 54(1): 241 - 245. [Abstract] [Full Text] [PDF]

				S. N. Parshina, R. Kleerebezem, J. L. Sanz, G. Lettinga, A. N. Nozhevnikova, N. A. Kostrikina, A. M. Lysenko, and A. J. M. Stams Soehngenia saccharolytica gen. nov., sp. nov. and Clostridium amygdalinum sp. nov., two novel anaerobic, benzaldehyde-converting bacteria Int J Syst Evol Microbiol, November 1, 2003; 53(6): 1791 - 1799. [Abstract] [Full Text] [PDF]

				M. Egert, B. Wagner, T. Lemke, A. Brune, and M. W. Friedrich Microbial Community Structure in Midgut and Hindgut of the Humus-Feeding Larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae) Appl. Envir. Microbiol., November 1, 2003; 69(11): 6659 - 6668. [Abstract] [Full Text] [PDF]

				D. Schmitt-Wagner, M. W. Friedrich, B. Wagner, and A. Brune Phylogenetic Diversity, Abundance, and Axial Distribution of Bacteria in the Intestinal Tract of Two Soil-Feeding Termites (Cubitermes spp.) Appl. Envir. Microbiol., October 1, 2003; 69(10): 6007 - 6017. [Abstract] [Full Text] [PDF]

				E. Miranda-Tello, M.-L. Fardeau, J. Sepulveda, L. Fernandez, J.-L. Cayol, P. Thomas, and B. Ollivier Garciella nitratireducens gen. nov., sp. nov., an anaerobic, thermophilic, nitrate- and thiosulfate-reducing bacterium isolated from an oilfield separator in the Gulf of Mexico Int J Syst Evol Microbiol, September 1, 2003; 53(5): 1509 - 1514. [Abstract] [Full Text] [PDF]

				H. Gest Names of bacteria and their evolutionary relationships Microbiology, August 1, 2003; 149(8): 1956 - 1958. [Full Text] [PDF]

				R. J. Wallace, N. McKain, N. R. McEwan, E. Miyagawa, L. C. Chaudhary, T. P. King, N. D. Walker, J. H. A. Apajalahti, and C. J. Newbold Eubacterium pyruvativorans sp. nov., a novel non-saccharolytic anaerobe from the rumen that ferments pyruvate and amino acids, forms caproate and utilizes acetate and propionate Int J Syst Evol Microbiol, July 1, 2003; 53(4): 965 - 970. [Abstract] [Full Text] [PDF]

				X. Cao, X. Liu, and X. Dong Alkaliphilus crotonatoxidans sp. nov., a strictly anaerobic, crotonate-dismutating bacterium isolated from a methanogenic environment Int J Syst Evol Microbiol, July 1, 2003; 53(4): 971 - 975. [Abstract] [Full Text] [PDF]

				G. L. Hold, A. Schwiertz, R. I. Aminov, M. Blaut, and H. J. Flint Oligonucleotide Probes That Detect Quantitatively Significant Groups of Butyrate-Producing Bacteria in Human Feces Appl. Envir. Microbiol., July 1, 2003; 69(7): 4320 - 4324. [Abstract] [Full Text] [PDF]

				S. Spring, B. Merkhoffer, N. Weiss, R. M. Kroppenstedt, H. Hippe, and E. Stackebrandt Characterization of novel psychrophilic clostridia from an Antarctic microbial mat: description of Clostridium frigoris sp. nov., Clostridium lacusfryxellense sp. nov., Clostridium bowmanii sp. nov. and Clostridium psychrophilum sp. nov. and reclassification of Clostridium laramiense as Clostridium estertheticum subsp. laramiense subsp. nov. Int J Syst Evol Microbiol, July 1, 2003; 53(4): 1019 - 1029. [Abstract] [Full Text] [PDF]

				N. Brisbarre, M.-L. Fardeau, V. Cueff, J.-L. Cayol, G. Barbier, V. Cilia, G. Ravot, P. Thomas, J.-L. Garcia, and B. Ollivier Clostridium caminithermale sp. nov., a slightly halophilic and moderately thermophilic bacterium isolated from an Atlantic deep-sea hydrothermal chimney Int J Syst Evol Microbiol, July 1, 2003; 53(4): 1043 - 1049. [Abstract] [Full Text] [PDF]

				A. I. Slobodkin, T. P. Tourova, N. A. Kostrikina, N. A. Chernyh, E. A. Bonch-Osmolovskaya, C. Jeanthon, and B. E. Jones Tepidibacter thalassicus gen. nov., sp. nov., a novel moderately thermophilic, anaerobic, fermentative bacterium from a deep-sea hydrothermal vent Int J Syst Evol Microbiol, July 1, 2003; 53(4): 1131 - 1134. [Abstract] [Full Text] [PDF]