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1Avian and Swine Respiratory Diseases Research Unit, National Animal Disease Center, Agricultural Research Service, US Department of Agriculture, PO Box 70, Ames, IA 50010, USA
2Department of Ecology & Evolutionary Biology, University of California at lrvine, Irvine, CA 92696, USA
Author for correspondence: Karin D. E. Everett. Tel: +1 706 542 5823. Fax: +1 706 542 5771. e-mail: keverett{at}calc.vet.uga.edu or kdeeverett{at}hotmail.com
ABSTRACT
The current taxonomic classification of Chlamydia is based on limited phenotypic, morphologic and genetic criteria. This classification does not take into account recent analysis of the ribosomal operon or recently identified obligately intracellular organisms that have a chlamydia-like developmental cycle of replication. Neither does it provide a systematic rationale for identifying new strains. In this study, phylogenetic analyses of the 16S and 23S rRNA genes are presented with corroborating genetic and phenotypic information to show that the order Chlamydiales contains at least four distinct groups at the family level and that within the Chlamydiaceae are two distinct lineages which branch into nine separate clusters. In this report a reclassification of the order Chlamydiales and its current taxa is proposed. This proposal retains currently known strains with > 90% 16S rRNA identity in the family Chlamydiaceae and separates other chlamydia-like organisms that have 80--90% 16S rRNA relatedness to the Chlamydiaceae into new families. Chlamydiae that were previously described as ‘Candidatus Parachlamydia acanthamoebae’ Amann, Springer, Schönhuber, Ludwig, Schmid, Müller and Michel 1997, become members of Parachlamydiaceae fam. nov., Parachlamydia acanthamoebae gen. nov., sp. nov. ‘Simkania’ strain Z becomes the founding member of Simkaniaceae fam. nov., Simkania negevensis gen. nov., sp. nov. The fourth group, which includes strain WSU 86--1044, was left unnamed. The Chlamydiaceae, which currently has only the genus Chlamydia, is divided into two genera, Chlamydia and Chlamydophila gen. nov. Two new species, Chlamydia muridarum sp. nov. and Chlamydia suis sp. nov., join Chlamydia trachomatis in the emended genus Chlamydia. Chlamydophila gen. nov. assimilates the current species, Chlamydia pecorum, Chlamydia pneumoniae and Chlamydia psittaci, to form Chlamydophila pecorum comb. nov., Chlamydophila pneumoniae comb. nov. and Chlamydophila psittaci comb. nov. Three new Chlamydophila species are derived from Chlamydia psittaci: Chlamydophila abortus gen. nov., sp. nov., Chlamydophila caviae gen. nov., sp. nov. and Chlamydophila felis gen. nov., sp. nov. Emended descriptions for the order Chlamydiales and for the family Chlamydiaceae are provided. These families, genera and species are readily distinguished by analysis of signature sequences in the 165 and 235 ribosomal genes.
Key Words: Chlamydiales • taxonomy • ribosomal • human pathogens • animal pathogens
The GenBank accession numbers for the sequences used in this paper are given in Figs 1 and 2 and Tables 2 and 3.
Present address: Department of Medical Microbiology and Parasitology, College of Veterinary Medicine, University of Georgia, Athens, GA 30602--7371, USA.
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T. Darville, J. M. O'Neill, C. W. Andrews Jr., U. M. Nagarajan, L. Stahl, and D. M. Ojcius Toll-Like Receptor-2, but Not Toll-Like Receptor-4, Is Essential for Development of Oviduct Pathology in Chlamydial Genital Tract Infection J. Immunol., December 1, 2003; 171(11): 6187 - 6197. [Abstract] [Full Text] [PDF]
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G. Greub, J.-L. Mege, and D. Raoult Parachlamydia acanthamoeba Enters and Multiplies within Human Macrophages and Induces Their Apoptosis Infect. Immun., October 1, 2003; 71(10): 5979 - 5985. [Abstract] [Full Text] [PDF]
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N. V. Guseva, S. T. Knight, J. D. Whittimore, and P. B. Wyrick Primary Cultures of Female Swine Genital Epithelial Cells In Vitro: a New Approach for the Study of Hormonal Modulation of Chlamydia Infection Infect. Immun., August 1, 2003; 71(8): 4700 - 4710. [Abstract] [Full Text] [PDF]
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B. Kocazeybek Chronic Chlamydophila pneumoniae infection in lung cancer, a risk factor: a case-control study J. Med. Microbiol., August 1, 2003; 52(8): 721 - 726. [Abstract] [Full Text] [PDF]
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E. Vretou, P. Giannikopoulou, D. Longbottom, and E. Psarrou Antigenic Organization of the N-Terminal Part of the Polymorphic Outer Membrane Proteins 90, 91A, and 91B of Chlamydophilaabortus Infect. Immun., June 1, 2003; 71(6): 3240 - 3250. [Abstract] [Full Text] [PDF]
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M. Van Loock, D. Vanrompay, B. Herrmann, J. Vander Stappen, G. Volckaert, B. M. Goddeeris, and K. D. E. Everett Missing links in the divergence of Chlamydophila abortus from Chlamydophila psittaci Int J Syst Evol Microbiol, May 1, 2003; 53(3): 761 - 770. [Abstract] [Full Text] [PDF]
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 T. D. Read, G. S. A. Myers, R. C. Brunham, W. C. Nelson, I. T. Paulsen, J. Heidelberg, E. Holtzapple, H. Khouri, N. B. Federova, H. A. Carty, et al. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae Nucleic Acids Res., April 15, 2003; 31(8): 2134 - 2147. [Abstract] [Full Text] [PDF]
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K. P. Karunakaran, Y. Noguchi, T. D. Read, A. Cherkasov, J. Kwee, C. Shen, C. C. Nelson, and R. C. Brunham Molecular Analysis of the Multiple GroEL Proteins of Chlamydiae J. Bacteriol., March 15, 2003; 185(6): 1958 - 1966. [Abstract] [Full Text] [PDF]
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 J.-L. Perfettini, D. M. Ojcius, C. W. Andrews Jr., S. J. Korsmeyer, R. G. Rank, and T. Darville Role of Proapoptotic BAX in Propagation of Chlamydia muridarum (the Mouse Pneumonitis Strain of Chlamydia trachomatis) and the Host Inflammatory Response J. Biol. Chem., March 7, 2003; 278(11): 9496 - 9502. [Abstract] [Full Text] [PDF]
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D. Longbottom, S. Fairley, S. Chapman, E. Psarrou, E. Vretou, and M. Livingstone Serological Diagnosis of Ovine Enzootic Abortion by Enzyme-Linked Immunosorbent Assay with a Recombinant Protein Fragment of the Polymorphic Outer Membrane Protein POMP90 of Chlamydophila abortus J. Clin. Microbiol., November 1, 2002; 40(11): 4235 - 4243. [Abstract] [Full Text] [PDF]
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E. P. C. Rocha, O. Pradillon, H. Bui, C. Sayada, and E. Denamur A new family of highly variable proteins in the Chlamydophila pneumoniae genome Nucleic Acids Res., October 15, 2002; 30(20): 4351 - 4360. [Abstract] [Full Text] [PDF]
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 M. Maurin, A. Bryskier, and D. Raoult Antibiotic Susceptibilities of Parachlamydia acanthamoeba in Amoebae Antimicrob. Agents Chemother., September 1, 2002; 46(9): 3065 - 3067. [Abstract] [Full Text] [PDF]
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S. Poppert, A. Essig, R. Marre, M. Wagner, and M. Horn Detection and Differentiation of Chlamydiae by Fluorescence In Situ Hybridization Appl. Envir. Microbiol., August 1, 2002; 68(8): 4081 - 4089. [Abstract] [Full Text] [PDF]
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E. Griffiths and R. S. Gupta Protein signatures distinctive of chlamydial species: horizontal transfers of cell wall biosynthesis genes glmU from archaea to chlamydiae and murA between chlamydiae and Streptomyces Microbiology, August 1, 2002; 148(8): 2541 - 2549. [Abstract] [Full Text] [PDF]
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F. S.L. Brinkman, J. L. Blanchard, A. Cherkasov, Y. Av-Gay, R. C. Brunham, R. C. Fernandez, B. B. Finlay, S. P. Otto, B.F. F. Ouellette, P. J. Keeling, et al. Evidence That Plant-Like Genes in Chlamydia Species Reflect an Ancestral Relationship between Chlamydiaceae, Cyanobacteria, and the Chloroplast Genome Res., August 1, 2002; 12(8): 1159 - 1167. [Abstract] [Full Text] [PDF]
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R. P. Morrison and H. D. Caldwell Immunity to Murine Chlamydial Genital Infection Infect. Immun., June 1, 2002; 70(6): 2741 - 2751. [Full Text] [PDF]
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J. S. Everson, S. A. Garner, B. Fane, B.-L. Liu, P. R. Lambden, and I. N. Clarke Biological Properties and Cell Tropism of Chp2, a Bacteriophage of the Obligate Intracellular Bacterium Chlamydophila abortus J. Bacteriol., May 15, 2002; 184(10): 2748 - 2754. [Abstract] [Full Text] [PDF]
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K. H. Wilson, W. J. Wilson, J. L. Radosevich, T. Z. DeSantis, V. S. Viswanathan, T. A. Kuczmarski, and G. L. Andersen High-Density Microarray of Small-Subunit Ribosomal DNA Probes Appl. Envir. Microbiol., May 1, 2002; 68(5): 2535 - 2541. [Abstract] [Full Text] [PDF]
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J.-L. Perfettini, T. Darville, A. Dautry-Varsat, R. G. Rank, and D. M. Ojcius Inhibition of Apoptosis by Gamma Interferon in Cells and Mice Infected with Chlamydia muridarum (the Mouse Pneumonitis Strain of Chlamydia trachomatis) Infect. Immun., May 1, 2002; 70(5): 2559 - 2565. [Abstract] [Full Text] [PDF]
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E. L. Marston, A. V. James, J. T. Parker, J. C. Hart, T. M. Brown, T. O. Messmer, D. L. Jue, C. M. Black, G. M. Carlone, E. W. Ades, et al. Newly Characterized Species-Specific Immunogenic Chlamydophila pneumoniae Peptide Reactive with Murine Monoclonal and Human Serum Antibodies Clin. Vaccine Immunol., March 1, 2002; 9(2): 446 - 452. [Abstract] [Full Text] [PDF]
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S. Kahane, N. Kimmel, and M. G. Friedman The growth cycle of Simkania negevensis Microbiology, March 1, 2002; 148(3): 735 - 742. [Abstract] [Full Text] [PDF]
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 M. Turmel, C. Otis, and C. Lemieux The Complete Mitochondrial DNA Sequence of Mesostigma viride Identifies This Green Alga as the Earliest Green Plant Divergence and Predicts a Highly Compact Mitochondrial Genome in the Ancestor of All Green Plants Mol. Biol. Evol., January 1, 2002; 19(1): 24 - 38. [Abstract] [Full Text] [PDF]
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E. Vretou, P. Giannikopoulou, and E. Psarrou Polymorphic outer-membrane proteins of Chlamydophila abortus are glycosylated Microbiology, December 1, 2001; 147(12): 3303 - 3310. [Abstract] [Full Text] [PDF]
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S. Kahane, B. Dvoskin, M. Mathias, and M. G. Friedman Infection of Acanthamoeba polyphaga with Simkania negevensis and S. negevensis Survival within Amoebal Cysts Appl. Envir. Microbiol., October 1, 2001; 67(10): 4789 - 4795. [Abstract] [Full Text]
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J. C. Hartley, S. Kaye, S. Stevenson, J. Bennett, and G. Ridgway PCR Detection and Molecular Identification of Chlamydiaceae Species J. Clin. Microbiol., September 1, 2001; 39(9): 3072 - 3079. [Abstract] [Full Text] [PDF]
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E. P. C. Rocha and A. Danchin Ongoing Evolution of Strand Composition in Bacterial Genomes Mol. Biol. Evol., September 1, 2001; 18(9): 1789 - 1799. [Abstract] [Full Text] [PDF]
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L. Del Rio, A. J. Buendia, J. Sanchez, M. C. Gallego, M. R. Caro, N. Ortega, J. Seva, F. J. Pallares, F. Cuello, and J. Salinas Endogenous Interleukin-12 Is Not Required for Resolution of Chlamydophila abortus (Chlamydia psittaci Serotype 1) Infection in Mice Infect. Immun., August 1, 2001; 69(8): 4808 - 4815. [Abstract] [Full Text] [PDF]
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C. Helps, N. Reeves, S. Tasker, and D. Harbour Use of Real-Time Quantitative PCR To Detect Chlamydophila felis Infection J. Clin. Microbiol., July 1, 2001; 39(7): 2675 - 2676. [Abstract] [Full Text] [PDF]
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 S.-Y. Yao, C. W. Stratton, W. M. Mitchell, and S. Sriram CSF oligoclonal bands in MS include antibodies against Chlamydophila antigens Neurology, May 8, 2001; 56(9): 1168 - 1176. [Abstract] [Full Text] [PDF]
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 G Entrican, D Buxton, and D Longbottom Chlamydial infection in sheep: immune control versus fetal pathology J R Soc Med, January 6, 2001; 94(6): 273 - 277. [Full Text] [PDF]
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S. A. Morre, J. M. Lyons, J. I. Ito Jr., and R. P. Morrison Murine Models of Chlamydia trachomatis Genital Tract Infection: Use of Mouse Pneumonitis Strain versus Human Strains Infect. Immun., December 1, 2000; 68(12): 7209 - 7211. [Full Text] [PDF]
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 L. Brade, A. Rozalski, P. Kosma, and H. Brade A monoclonal antibody recognizing the 3-deoxy-D-manno-oct-2-ulosonic acid (Kdo) trisaccharide {alpha}Kdo(2->4){alpha}Kdo(2->4){alpha}Kdo of Chlamydophila spacepsittaci 6BC lipopolysaccharide Innate Immunity, October 1, 2000; 6(5): 361 - 368. [Abstract] [PDF]
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A. T. Bull, A. C. Ward, and M. Goodfellow Search and Discovery Strategies for Biotechnology: the Paradigm Shift Microbiol. Mol. Biol. Rev., September 1, 2000; 64(3): 573 - 606. [Abstract] [Full Text] [PDF]
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B. Herrmann, R. Rahman, S. Bergström, J. Bonnedahl, and B. Olsen Chlamydophila abortus in a Brown Skua (Catharacta antarctica lonnbergi) from a Subantarctic Island Appl. Envir. Microbiol., August 1, 2000; 66(8): 3654 - 3656. [Abstract] [Full Text]
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M. Shirai, H. Hirakawa, M. Kimoto, M. Tabuchi, F. Kishi, K. Ouchi, T. Shiba, K. Ishii, M. Hattori, S. Kuhara, et al. Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA Nucleic Acids Res., June 15, 2000; 28(12): 2311 - 2314. [Abstract] [Full Text] [PDF]
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