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Chapter 40 : Molecular Evolution of Chlamydiales

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Molecular Evolution of Chlamydiales, Page 1 of 2

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Abstract:

Organisms of the order Chlamydiales comprise a group of obligate intracellular pathogens of ever-growing importance and number. Over the past six years, comparative analyses of complete chlamydial genome sequences have provided an explosive amount of data that have led to important new hypotheses regarding the molecular origins of Chlamydiales. It was surprising that Chlamydiales had many proteins that were similar to plant proteins targeted to the chloroplast. Protease-like activating factor (CPAF) is unique to Chlamydiales and likely critical to host adaptive immunity. Many of the gene differences identified are clustered into discrete regions including the replication termination region terminus or the plasticity zone (PZ), the two clusters plus PmpD of polymorphic membrane proteins (Pmp), the transmembrane head (TMH)/Inc protein cluster, and the biotin biosynthetic operon. Some of the most interesting data on Inc proteins has come from Chlamydiales genomic comparisons, where 20 open reading frames were identified for the genus Chlamydia. Studying the genetic variability of multiple genes encoded by chlamydial genomes has resulted in insights into the molecular evolution of this organism. Researchers have focused on the comparative genetics of genes with sufficient genetic variation or those with specialized structural or housekeeping functions. From these studies, a number of findings are revealing the mechanisms by which Chlamydiales diverge.

Citation: Dean D, Millman K. 2008. Molecular Evolution of Chlamydiales, p 475-488. In Baquero F, Nombela C, Cassell G, Gutiérrez-Fuentes J (ed), Evolutionary Biology of Bacterial and Fungal Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815639.ch40
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References

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1. Allen, J. E.,, R. M. Locksley, and, R. S. Stephens. 1991. A single peptide from the major outer membrane protein of Chlamydia trachomatis elicits T cell help for the production of antibodies to protective determinants. J. Immunol. 147:674679.
2. Altschul, S. F.,, T. L. Madden,, A. A. Schaffer,, J. Zhang,, Z. Zhang,, W. Miller, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:33893402.
3. Amann, R.,, N. Springer,, W. Schonhuber,, W. Ludwig,, E. N. Schmid,, K. D. Muller, et al. 1997. Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp. Appl. Environ. Microbiol. 63:115121.
4. Andersson, S. G.,, A. Zomorodipour,, J. O. Andersson,, T. Sicheritz-Ponten,, U. C. Alsmark,, R. M. Podowski, et al. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396:133140.
5. Barnes, R. C.,, A. M. Rompalo, and, W. E. Stamm. 1987. Comparison of Chlamydia trachomatis serovars causing rectal and cervical infections. J. Infect. Dis. 156:953958.
6. Bauwens, J. E.,, M. F. Lampe,, R. J. Suchland,, K. Wong, and, W. E. Stamm. 1995. Infection with Chlamydia trachomatis lymphogranuloma venereum serovar L1 in homosexual men with proctitis: molecular analysis of an unusual case cluster. Clin. Infect. Dis. 20:576581.
7. Beatty, W. L.,, R. P. Morrison, and, G. I. Byrne. 1994. Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol. Rev. 58:686699.
8. Belland, R. J.,, M. A. Scidmore,, D. D. Crane,, D. M. Hogan,, W. Whitmire,, G. McClarty, et al. 2001. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes. Proc. Natl. Acad. Sci. USA 98:1398413989.
9. Blanchard, J. L., and, M. Lynch. 2000. Organellar genes: why do they end up in the nucleus? Trends Genet. 16:315320.
10. Braun, J.,, M. Grolms,, A. Distler, and, J. Sieper. 1994. The specific antibacterial proliferation of reactive arthritis synovial T cells is not due to their higher proportion of CD45RO cells compared to peripheral blood. J. Rheumatol. 21:17021707.
11. Brinkman, F. S.,, J. L. Blanchard,, A. Cherkasov,, Y. Av-Gay,, R. C. Brunham,, R. C. Fernandez, et al. 2002. Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res. 12:11591167.
12. Brunham, R.,, C. Yang,, I. Maclean,, J. Kimani,, G. Maitha, and, F. Plummer. 1994. Chlamydia trachomatis from individuals in a sexually transmitted diseases core group exhibit frequent sequence variation in the major outer membrane protein (omp1) gene. J. Clin. Invest. 94:458463.
13. Campbell, L. A.,, C. C. Kuo,, S. P. Wang, and, J. T. Grayston. 1990. Serological response to Chlamydia pneumoniae infection. J. Clin. Microbiol. 28:12611264.
14. Carlson, J. H.,, S. Hughes,, D. Hogan,, G. Cieplak,, D. E. Sturdevant,, G. McClarty, et al. 2004. Polymorphisms in the Chlamydia trachomatis cytotoxin locus associated with ocular and genital isolates. Infect. Immun. 72:70637072.
15. Ceravolo, I. P.,, A. C. Chaves,, C. A. Bonjardim,, D. Sibley,, A. J. Romanha, and, R. T. Gazzinelli. 1999. Replication of Toxo-plasma gondii, but not Trypanosoma cruzi, is regulated in human fibroblasts activated with gamma interferon: requirement of a functional JAK/STAT pathway. Infect. Immun. 67:22332240.
16. Cevenini, R.,, M. Donati,, E. Brocchi,, F. De Simone, and, M. La Placa. 1991. Partial characterization of an 89-kDa highly immunoreactive protein from Chlamydia psittaci A/22 causing ovine abortion. FEMS Microbiol. Lett. 65:111115.
17. Chalmers, R., and, M. Blot. 1999. Insertion sequences and transposons, p. 151168. In R. L. Charlebois (ed.), Organization of the Prokaryotic Genome. ASM Press, Washington, DC.
18. Corsaro, D., and, D. Venditti. 2004. Emerging chlamydial infections. Crit. Rev. Microbiol. 30:75106.
19. Dean, D.,, E. Oudens,, G. Bolan,, N. Padian, and, J. Schachter. 1995a. Major outer membrane protein variants of Chlamydia trachomatis are associated with severe upper genital tract infections and histopathology in San Francisco. J. Infect. Dis. 172:10131022.
20. Dean, D.,, J. Schachter,, C. R. Dawson, and, R. S. Stephens. 1992. Comparison of the major outer membrane protein variant sequence regions of B/Ba isolates: a molecular epidemiologic approach to Chlamydia trachomatis infections. J. Infect. Dis. 166:383392.
21. Dean, D.,, A. Shama,, J. Schachter, and, C. R. Dawson. 1995b. Molecular identification of an avian strain of Chlamydia psittaci causing severe keratoconjunctivitis in a bird fancier. Clin. Infect. Dis. 20:11791185.
22. Dean, D.,, R. Suchland, and, W. Stamm. 2000. Evidence for long-term cervical persistence of Chlamydia trachomatis by omp1 genotyping. J. Infect. Dis. 182:909916.
23. Dean, D. Chlamydia trachomatis sexually transmitted diseases, p. 473490. In D. H. Connor,, D. A. Schwartz, and, F. W. Chandler (ed.), Pathology of Infectious Diseases. Appleton and Lange, Stamford, CT.
24. Dean, D. 1994. Molecular characterization of new Chlamydia trachomatis serological variants from a trachoma endemic region of Africa, p. 259262. In J. Orfila,, G. I. Byrne,, M. A. Chernesky,, J. T. Grayston,, R. B. Jones,, G. L. Ridgway, et al. (ed.), Chlamydial Infections. Societa Editrice Esculapio, Bologna, Italy.
25. Dean, D. 2002. Pathogenesis of chlamydial ocular infections, p. 122. In W. Tasman, and, E. A. Jaeger (ed.), Duane’s Foundations of Clinical Ophthalmology. Lippincott Williams & Wilkins, Philadelphia, PA.
26. Dugan, J.,, D. D. Rockey,, L. Jones, and, A. A. Andersen. 2004. Tetracycline resistance in Chlamydia suis mediated by genomic islands inserted into the chlamydial inv-like gene. Anti-microb. Agents Chemother. 48:39893995.
27. Everett, K. D.,, R. M. Bush, and, A. A. Andersen. 1999. Emended description of the order Chlamydiales, proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. Int. J. Syst. Bacteriol. 49:415440.
28. Everett, K. D. 2000. Chlamydia and Chlamydiales: more than meets the eye. Vet. Microbiol. 75:109126.
29. Everson, J. S.,, S. A. Garner,, B. Fane,, B. L. Liu,, P. R. Lambden, and, I. N. Clarke. 2002. Biological properties and cell tropism of Chp2, a bacteriophage of the obligate intracellular bacterium Chlamydophila abortus. J. Bacteriol. 184:27482754.
30. Fehlner-Gardiner, C.,, C. Roshick,, J. H. Carlson,, S. Hughes,, R. J. Belland,, H. D. Caldwell, et al. 2002. Molecular basis defining human Chlamydia trachomatis tissue tropism. A possible role for tryptophan synthase. J. Biol. Chem. 277:2689326903.
31. Fitch, W. M.,, E. M. Peterson, and, L. M. de la Maza. 1993. Phylogenetic analysis of the outer-membrane-protein genes of Chlamydiae, and its implication for vaccine development. Mol. Biol. Evol. 10:892913.
32. Friedman, M. G.,, B. Dvoskin, and, S. Kahane. 2003. Infections with the chlamydia-like microorganism Simkania negevensis, a possible emerging pathogen. Microbes Infect. 5:10131021.
33. Fritsche, T. R.,, M. Horn,, M. Wagner,, R. P. Herwig,, K. H. Schleifer, and, R. K. Gautom. 2000. Phylogenetic diversity among geographically dispersed Chlamydiales endosymbionts recovered from clinical and environmental isolates of Acanthamoeba spp. Appl. Environ. Microbiol. 66:26132619.
34. Frost, E. H.,, S. Deslandes,, D. Gendron,, D. Bourgaux-Ramoisy, and, P. Bourgaux. 1995. Variation outside variable segments of the major outer membrane protein distinguishes trachoma from urogenital isolates of the same serovar of Chlamydia trachomatis. Genitourin. Med. 71:1823.
35. Garner, S. A.,, J. S. Everson,, P. R. Lambden,, B. A. Fane, and, I. N. Clarke. 2004. Isolation, molecular characterisation and genome sequence of a bacteriophage (Chp3) from Chlamydophila pecorum. Virus Genes 28:207214.
36. Girjes, A. A.,, F. N. Carrick, and, M. F. Lavin. 1994. Remarkable sequence relatedness in the DNA encoding the major outer membrane protein of Chlamydia psittaci (koala type I) and Chlamydia pneumoniae. Gene 138:139142.
37. Gomes, J. P.,, W. J. Bruno,, M. J. Borrego, and, D. Dean. 2004. Recombination in the genome of Chlamydia trachomatis involving the polymorphic membrane protein C gene relative to ompA and evidence for horizontal gene transfer. J. Bacteriol. 186:42954306.
38. Gomes, J. P.,, A. Nunes,, W. J. Bruno,, M. J. Borrego,, C. Florindo, and, D. Dean. 2006. Polymorphisms in the nine polymorphic membrane proteins of Chlamydia trachomatis across all serovars: evidence for serovar Da recombination and correlation with tissue tropism. J. Bacteriol. 188:275286.
39. Gray, M. W., and, B. F. Lang. 1998. Transcription in chloroplasts and mitochondria: a tale of two polymerases. Trends Microbiol. 6:13.
40. Griffiths, E., and, R. S. Gupta. 2002. 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 148:25412549.
41. Griffiths, E.,, A. K. Petrich, and, R. S. Gupta. 2005. Conserved indels in essential proteins that are distinctive characteristics of Chlamydiales and provide novel means for their identification. Microbiology 151:26472657.
42. Griffiths, E.,, M. S. Ventresca, and, R. S. Gupta. 2006. BLAST screening of chlamydial genomes to identify signature proteins that are unique for the Chlamydiales, Chlamydiaceae, Chlamydophila and Chlamydia groups of species. BMC Genomics 7:14.
43. Grimwood, J., and, R. S. Stephens. 1999. Computational analysis of the polymorphic membrane protein superfamily of Chlamydia trachomatis and Chlamydia pneumoniae. Microb. Comp. Genomics 4:187201.
44. Hackstadt, T. 1999. Cell biology, p. 101138. In R. S. Stephens (ed.), Chlamydia: Intracellular Biology, Pathogenesis and Immunity. ASM Press, Washington, DC.
45. Hallet, B.,, R. Rezsohazy,, J. Mahillon, and, J. Delcour. 1994. IS231A insertion specificity: consensus sequence and DNA bending at the target site. Mol. Microbiol. 14:131139.
46. Hammerschmidt, S.,, R. Hilse,, J. P. van Putten,, R. Gerardy-Schahn,, A. Unkmeir, and, M. Frosch. 1996. Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J. 15:192198.
47. Hayes, L. J.,, S. Pecharatana,, R. L. Bailey,, T. J. Hampton,, M. A. Pickett,, D. C. Mabey, et al. 1995. Extent and kinetics of genetic change in the omp1 gene of Chlamydia trachomatis in two villages with endemic trachoma. J. Infect. Dis. 172:268272.
48. Henderson, I. R., and, A. C. Lam. 2001. Polymorphic proteins of Chlamydia spp.—autotransporters beyond the Proteobacteria. Trends Microbiol. 9:573578.
49. Hintz, N. J.,, D. G. Ennis,, W. F. Liu, and, S. H. Larsen. 1995. The recA gene of Chlamydia trachomatis: cloning, sequence, and characterization in Escherichia coli. FEMS Microbiol. Lett. 127:175180.
50. Hodgkin, P. D. 1997. An antigen valence theory to explain the evolution and organization of the humoral immune response. Immunol. Cell Biol. 75:604618.
51. Horn, M.,, A. Collingro,, S. Schmitz-Esser,, C. L. Beier,, U. Purkhold,, B. Fartmann, et al. 2004. Illuminating the evolutionary history of chlamydiae. Science 304:728730.
52. Horn, M.,, M. Wagner,, K. D. Muller,, E. N. Schmid,, T. R. Fritsche,, K. H. Schleifer, et al. 2000. Neochlamydia hartmannellae gen. nov., sp. nov. (Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformis. Microbiology 146:12311239.
53. Horn, M., and, M. Wagner. 2001. Evidence for additional genus-level diversity of Chlamydiales in the environment. FEMS Microbiol. Lett. 204:7174.
54. Hsia, R.,, H. Ohayon,, P. Gounon,, A. Dautry-Varsat, and, P. M. Bavoil. 2000a. Phage infection of the obligate intracellular bacterium, Chlamydia psittaci strain guinea pig inclusion conjunctivitis. Microbes Infect. 2:761772.
55. Hsia, R. C., and, P. M. Bavoil. 1996. Homologs of Escherichia coli recJ, gltX and of a putative ‘early’ gene of avian Chlamydia psittaci are located upstream of the ‘late’ omp2 locus of Chlamydia psittaci strain guinea pig inclusion conjunctivitis. Gene 176:163169.
56. Hsia, R. C.,, L. M. Ting, and, P. M. Bavoil. 2000b. Microvirus of Chlamydia psittaci strain guinea pig inclusion conjunctivitis: isolation and molecular characterization. Microbiology 146:16511660.
57. Hyde, C. C., and, E. W. Miles. 1990. The tryptophan synthase multienzyme complex: exploring structure-function relationships with X-ray crystallography and mutagenesis. Biotechnology 8:2732.
58. Isberg, R. R.,, D. L. Voorhis, and, S. Falkow. 1987. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50:769778.
59. Ishizaki, M.,, J. E. Allen,, P. R. Beatty, and, R. S. Stephens. 1992. Immune specificity of murine T-cell lines to the major outer membrane protein of Chlamydia trachomatis. Infect. Immun. 60:37143718.
60. Kahane, S.,, D. Greenberg,, M. G. Friedman,, H. Haikin, and, R. Dagan. 1998. High prevalence of “Simkania Z,” a novel Chlamydia-like bacterium, in infants with acute bronchiolitis. J. Infect. Dis. 177:14251429.
61. Kalman, S.,, W. Mitchell,, R. Marathe,, C. Lammel,, J. Fan,, R. W. Hyman, et al. 1999. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21:385389.
62. Karunakaran, K. P.,, J. F. Blanchard,, A. Raudonikiene,, C. X. Shen,, A. D. Murdin, and, R. C. Brunham. 2002. Molecular detection and seroepidemiology of the Chlamydia pneumoniae bacteriophage (Phi Cpn1). J. Clin. Microbiol. 40:40104014.
63. Kersulyte, D.,, N. S. Akopyants,, S. W. Clifton,, B. A. Roe, and, D. E. Berg. 1998. Novel sequence organization and insertion specificity of IS605 and IS606: chimaeric transposable elements of Helicobacter pylori. Gene 223:175186.
64. Knudsen, K.,, A. S. Madsen,, P. Mygind,, G. Christiansen, and, S. Birkelund. 1999. Identification of two novel genes encoding 97- to 99-kilodalton outer membrane proteins of Chlamydia pneumoniae. Infect. Immun. 67:375383.
65. Lampe, M. F.,, R. J. Suchland, and, W. E. Stamm. 1993. Nucleotide sequence of the variable domains within the major outer membrane protein gene from serovariants of Chlamydia trachomatis. Infect. Immun. 61:213219.
66. Lange, B. M.,, T. Rujan,, W. Martin, and, R. Croteau. 2000. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci. USA 97:1317213177.
67. Lin, J. S.,, S. P. Donegan,, T. C. Heeren,, M. Greenberg,, E. E. Flaherty,, R. Haivanis, et al. 1998. Transmission of Chlamydia trachomatis and Neisseria gonorrhoeae among men with urethritis and their female sex partners. J. Infect. Dis. 178:17071712.
68. Liu, B. L.,, J. S. Everson,, B. Fane,, P. Giannikopoulou,, E. Vretou,, P. R. Lambden, et al. 2000. Molecular characterization of a bacteriophage (Chp2) from Chlamydia psittaci. J. Virol. 74:34643469.
69. Liu, H.,, Y. Hwangbo,, S. Holte,, J. Lee,, C. Wang,, N. Kaupp, et al. 2004. Analysis of genetic polymorphisms in CCR5, CCR2, stromal cell-derived factor-1, RANTES, and dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin in seronegative individuals repeatedly exposed to HIV-1. J. Infect. Dis. 190:10551058.
70. Longbottom, D., and, L. J. Coulter. 2003. Animal chlamydioses and zoonotic implications. J. Comp. Pathol. 128:217244.
71. Lundblad, V.,, A. F. Taylor,, G. R. Smith, and, N. Kleckner. 1984. Unusual alleles of recB and recC stimulate excision of inverted repeat transposons Tn10 and Tn5. Proc. Natl. Acad. Sci. USA 81:824828.
72. Mahillon, J., and, M. Chandler. 1998. Insertion sequences. Microbiol. Mol. Biol. Rev. 62:725774.
73. Mendiola, M. V., and, F. de la Cruz. 1989. Specificity of insertion of IS91, an insertion sequence present in alpha-haemolysin plasmids of Escherichia coli. Mol. Microbiol. 3:979984.
74. Millman, K.,, C. M. Black,, R. E. Johnson,, W. E. Stamm,, R. B. Jones,, E. W. Hook, et al. 2004. Population-based genetic and evolutionary analysis of Chlamydia trachomatis urogenital strain variation in the United States. J. Bacteriol. 186:24572465.
75. Millman, K. L.,, S. Tavare, and, D. Dean. 2001. Recombination in the ompA gene but not the omcB gene of Chlamydia contributes to serovar-specific differences in tissue tropism, immune surveillance, and persistence of the organism. J. Bacteriol. 183:59976008.
76. Moulder, J. W. 1991. Interaction of chlamydiae and host cells in vitro. Microbiol. Rev. 55:143190.
77. Nagata, S.,, C. C. Hyde, and, E. W. Miles. 1989. The alpha subunit of tryptophan synthase. Evidence that aspartic acid 60 is a catalytic residue and that the double alteration of residues 175 and 211 in a second-site revertant restores the proper geometry of the substrate binding site. J. Biol. Chem. 264:62886296.
78. Ossewaarde, J. M., and, A. Meijer. 1999. Molecular evidence for the existence of additional members of the order Chlamydiales. Microbiology 145:411417.
79. Radnedge, L.,, P. G. Agron,, P. L. Worsham, and, G. L. Andersen. 2002. Genome plasticity in Yersinia pestis. Microbiology 148:16871698.
80. Ramsey, K. H.,, W. J. T. Newhall, and, R. G. Rank. 1989. Humoral immune response to chlamydial genital infection of mice with the agent of mouse pneumonitis. Infect. Immun. 57:24412446.
81. Rasmussen, S. J.,, P. Timms,, P. R. Beatty, and, R. S. Stephens. 1996. Cytotoxic-T-lymphocyte-mediated cytolysis of L cells persistently infected with Chlamydia spp. Infect. Immun. 64:19441949.
82. Read, T. D.,, R. C. Brunham,, C. Shen,, S. R. Gill,, J. F. Heidelberg,, O. White, et al. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:13971406.
83. Read, T. D.,, G. S. Myers,, R. C. Brunham,, W. C. Nelson,, I. T. Paulsen,, J. Heidelberg, et al. 2003. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res. 31:21342147.
84. Reumann, S., and, K. Keegstra. 1999. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci. 4:302307.
85. Ridderhof, J. C., and, R. C. Barnes. 1989. Fusion of inclusions following superinfection of HeLa cells by two serovars of Chlamydia trachomatis. Infect. Immun. 57:31893193.
86. Royo, J.,, E. Gimez, and, G. Hueros. 2000. CMP-KDO synthetase: a plant gene borrowed from gram-negative eubacteria. Trends Genet 16:432433.
87. Rujan, T., and, W. Martin. 2001. How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. Trends Genet. 17:113120.
88. Rurangirwa, F. R.,, P. M. Dilbeck,, T. B. Crawford,, T. C. McGuire, and, T. F. McElwain. 1999. Analysis of the 16S rRNA gene of microorganism WSU 86-1044 from an aborted bovine foetus reveals that it is a member of the order Chlamydiales: proposal of Waddliaceae fam. nov., Waddlia chondrophila gen. nov., sp. nov. Int. J. Syst. Bacteriol. 49:577581.
89. Saikku, P.,, S. P. Wang,, M. Kleemola,, E. Brander,, E. Rusanen, and, J. T. Grayston. 1985. An epidemic of mild pneumonia due to an unusual strain of Chlamydia psittaci. J. Infect. Dis. 151:832839.
90. Saikku, P. 1999. Epidemiology of Chlamydia pneumoniae in atherosclerosis. Am. Heart J. 138:S500S503.
91. Salvatore, P.,, C. Pagliarulo,, R. Colicchio,, P. Zecca,, G. Cantalupo,, M. Tredici, et al. 2001. Identification, characterization, and variable expression of a naturally occurring inhibitor protein of IS1106 transposase in clinical isolates of Neisseria meningitidis. Infect. Immun. 69:74257436.
92. Scidmore-Carlson, M. A.,, E. I. Shaw,, C. A. Dooley,, E. R. Fischer, and, T. Hackstadt. 1999. Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins. Mol. Microbiol. 33:753765.
93. Sexually Transmitted Disease Surveillance. 2004. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, GA.
94. Shaw, A. C.,, G. Christiansen,, P. Roepstorff, and, S. Birkelund. 2000. Genetic differences in the Chlamydia trachomatis tryptophan synthase alpha-subunit can explain variations in serovar pathogenesis. Microbes Infect. 2:581592.
95. Shaw, A. C.,, K. Gevaert,, H. Demol,, B. Hoorelbeke,, J. Vandekerckhove,, M. R. Larsen, et al. 2002a. Comparative proteome analysis of Chlamydia trachomatis serovar A, D and L2. Proteomics 2:164186.
96. Shaw, A. C.,, B. B. Vandahl,, M. R. Larsen,, P. Roepstorff,, K. Gevaert,, J. Vandekerckhove, et al. 2002b. Characterization of a secreted Chlamydia protease. Cell Microbiol. 4:411424.
97. Shirai, M.,, H. Hirakawa,, M. Kimoto,, M. Tabuchi,, F. Kishi,, K. Ouchi, et al. 2000a. Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA. Nucleic Acids Res. 28:23112314.
98. Shirai, M.,, H. Hirakawa,, K. Ouchi,, M. Tabuchi,, F. Kishi,, M. Kimoto, et al. 2000b. Comparison of outer membrane protein genes omp and pmp in the whole genome sequences of Chlamydia pneumoniae isolates from Japan and the United States. J. Infect. Dis. 181(Suppl 3): S524S527.
99. Skipp, P.,, J. Robinson,, C. D. O’Connor, and, I. N. Clarke. 2005. Shotgun proteomic analysis of Chlamydia trachomatis. Proteomics 5:15581573.
100. Stephens, R. S.,, S. Kalman,, C. Lammel,, J. Fan,, R. Marathe,, L. Aravind, et al. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754759.
101. Storey, C.,, M. Lusher,, P. Yates, and, S. Richmond. 1993. Evidence for Chlamydia pneumoniae of non-human origin. J. Gen. Microbiol. 139:26212626.
102. Tanzer, R. J., and, T. P. Hatch. 2001. Characterization of outer membrane proteins in Chlamydia trachomatis LGV serovar L2. J. Bacteriol. 183:26862690.
103. Telfer, B. L.,, S. A. Moberley,, K. P. Hort,, J. M. Branley,, D. E. Dwyer,, D. J. Muscatello, et al. 2005. Probable psittacosis outbreak linked to wild birds. Emerg. Infect. Dis. 11:391397.
104. Thomson, N. R.,, C. Yeats,, K. Bell,, M. T. Holden,, S. D. Bentley,, M. Livingstone, et al. 2005. The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res. 15:629640.
105. Wang, S. P., and, J. T. Grayston. 1991. Serotyping of Chlamydia trachomatis by indirect fluorescent-antibody staining of inclusions in cell culture with monoclonal antibodies. J. Clin. Microbiol. 29:12951298.
106. Weeden, N. F. 1981. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J. Mol. Evol. 17:133139.
107. Yang, C. L.,, I. Maclean, and, R. C. Brunham. 1993. DNA sequence polymorphism of the Chlamydia trachomatis omp1 gene. J. Infect. Dis. 168:12251230.
108. Zhang, D. J.,, H. Fan,, G. McClarty, and, R. C. Brunham. 1995. Identification of the Chlamydia trachomatis RecA-encoding gene. Infect. Immun. 63:676680.

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