1932

Abstract

Species of are the etiologic agent of endemic blinding trachoma, the leading cause of bacterial sexually transmitted diseases, significant respiratory pathogens, and a zoonotic threat. Their dependence on an intracellular growth niche and their peculiar developmental cycle are major challenges to elucidating their biology and virulence traits. The last decade has seen tremendous advances in our ability to perform a molecular genetic analysis of species. Major achievements include the generation of large collections of mutant strains, now available for forward- and reverse-genetic applications, and the introduction of a system for plasmid-based transformation enabling complementation of mutations; expression of foreign, modified, or reporter genes; and even targeted gene disruptions. This review summarizes the current status of the molecular genetic toolbox for species and highlights new insights into their biology and new challenges in the nascent field of genetics.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-102215-095539
2016-09-08
2024-06-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/70/1/annurev-micro-102215-095539.html?itemId=/content/journals/10.1146/annurev-micro-102215-095539&mimeType=html&fmt=ahah

Literature Cited

  1. Abdelrahman YM, Belland RJ. 1.  2005. The chlamydial developmental cycle. FEMS Microbiol. Rev. 29:949–59 [Google Scholar]
  2. Agaisse H, Derre I. 2.  2013. A C. trachomatis cloning vector and the generation of C. trachomatis strains expressing fluorescent proteins under the control of a C. trachomatis promoter. PLOS ONE 8:e57090 [Google Scholar]
  3. Albrecht M, Sharma CM, Reinhardt R, Vogel J, Rudel T. 3.  2010. Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome. Nucleic Acids Res. 38:868–77 [Google Scholar]
  4. Arnold R, Brandmaier S, Kleine F, Tischler P, Heinz E. 4.  et al. 2009. Sequence-based prediction of type III secreted proteins. PLOS Pathog. 5:e1000376 [Google Scholar]
  5. Azuma Y, Hirakawa H, Yamashita A, Cai Y, Rahman MA. 5.  et al. 2006. Genome sequence of the cat pathogen, Chlamydophila felis. DNA Res. 13:15–23 [Google Scholar]
  6. Barta ML, Battaile KP, Lovell S, Hefty PS. 6.  2015. Hypothetical protein CT398 (CdsZ) interacts with σ54 (RpoN)-holoenzyme and the type III secretion export apparatus in Chlamydia trachomatis. Protein Sci. 24:1617–32 [Google Scholar]
  7. Bastidas RJ, Valdivia RH. 7.  2016. Emancipating Chlamydia: advances in genetic engineering of a recalcitrant intracellular pathogen. Microbiol. Mol. Biol. Rev. 80:411–27 [Google Scholar]
  8. Batteiger BE, Wan R, Williams JA, He L, Ma A. 8.  et al. 2014. Novel Chlamydia trachomatis strains in heterosexual sex partners, Indianapolis, Indiana, USA. Emerg. Infect. Dis. 20:1841–47 [Google Scholar]
  9. Bauler LD, Hackstadt T. 9.  2014. Expression and targeting of secreted proteins from Chlamydia trachomatis. J. Bacteriol. 196:1325–34 [Google Scholar]
  10. Beare PA, Howe D, Cockrell DC, Omsland A, Hansen B, Heinzen RA. 10.  2009. Characterization of a Coxiella burnetii ftsZ mutant generated by Himar1 transposon mutagenesis. J. Bacteriol. 191:1369–81 [Google Scholar]
  11. Beare PA, Larson CL, Gilk SD, Heinzen RA. 11.  2012. Two systems for targeted gene deletion in Coxiella burnetii. Appl. Environ. Microbiol. 78:4580–89 [Google Scholar]
  12. Belland RJ, Zhong G, Crane DD, Hogan D, Sturdevant D. 12.  et al. 2003. Genomic transcriptional profiling of the developmental cycle of Chlamydia trachomatis. PNAS 100:8478–83 [Google Scholar]
  13. Betts HJ, Wolf K, Fields KA. 13.  2009. Effector protein modulation of host cells: examples in the Chlamydia spp. arsenal. Curr. Opin. Microbiol. 12:81–87 [Google Scholar]
  14. Binet R, Maurelli AT. 14.  2009. Transformation and isolation of allelic exchange mutants of Chlamydia psittaci using recombinant DNA introduced by electroporation. PNAS 106:292–97 [Google Scholar]
  15. Borges V, Pinheiro M, Antelo M, Sampaio DA, Vieira L. 15.  et al. 2015. Chlamydia trachomatis in vivo to in vitro transition reveals mechanisms of phase variation and down-regulation of virulence factors. PLOS ONE 10:e0133420 [Google Scholar]
  16. Brown HM, Knowlton AE, Snavely E, Nguyen BD, Richards TS, Grieshaber SS. 16.  2014. Multinucleation during C. trachomatis infections is caused by the contribution of two effector pathways. PLOS ONE 9:e100763 [Google Scholar]
  17. Brunham R, Yang C, Maclean I, Kimani J, Maitha G, Plummer F. 17.  1994. Chlamydia trachomatis from individuals in a sexually transmitted disease core group exhibit frequent sequence variation in the major outer membrane protein (omp1) gene. J. Clin. Investig. 94:458–63 [Google Scholar]
  18. Burillo A, Bouza E. 18.  2010. Chlamydophila pneumoniae. Infect. Dis. Clin. North Am. 24:61–71 [Google Scholar]
  19. Campbell J, Huang Y, Liu Y, Schenken R, Arulanandam B, Zhong G. 19.  2014. Bioluminescence imaging of Chlamydia muridarum ascending infection in mice. PLOS ONE 9:e101634 [Google Scholar]
  20. Carlson JH, Porcella SF, McClarty G, Caldwell HD. 20.  2005. Comparative genomic analysis of Chlamydia trachomatis oculotropic and genitotropic strains. Infect. Immun. 73:6407–18 [Google Scholar]
  21. Carlson JH, Whitmire WM, Crane DD, Wicke L, Virtaneva K. 21.  et al. 2008. The Chlamydia trachomatis plasmid is a transcriptional regulator of chromosomal genes and a virulence factor. Infect. Immun. 76:2273–83 [Google Scholar]
  22. Chen AL, Johnson KA, Lee JK, Sutterlin C, Tan M. 22.  2012. CPAF: a chlamydial protease in search of an authentic substrate. PLOS Pathog. 8:e1002842 [Google Scholar]
  23. Chen C, Zhong G, Ren L, Lu C, Li Z, Wu Y. 23.  2015. Identification of plasmid-free Chlamydia muridarum organisms using a Pgp3 detection-based immunofluorescence assay. J. Microbiol. Biotechnol. 25:1621–28 [Google Scholar]
  24. Chen C, Zhou Z, Conrad T, Yang Z, Dai J. 24.  et al. 2015. In vitro passage selects for Chlamydia muridarum with enhanced infectivity in cultured cells but attenuated pathogenicity in mouse upper genital tract. Infect. Immun. 83:1881–92 [Google Scholar]
  25. Chen YS, Bastidas RJ, Saka HA, Carpenter VK, Richards KL. 25.  et al. 2014. The Chlamydia trachomatis type III secretion chaperone Slc1 engages multiple early effectors, including TepP, a tyrosine-phosphorylated protein required for the recruitment of CrkI-II to nascent inclusions and innate immune signaling. PLOS Pathog. 10:e1003954 [Google Scholar]
  26. Cheng E, Tan M. 26.  2012. Differential effects of DNA supercoiling on Chlamydia early promoters correlate with expression patterns in midcycle. J. Bacteriol. 194:3109–15 [Google Scholar]
  27. Christian J, Vier J, Paschen SA, Hacker G. 27.  2010. Cleavage of the NF-κB family protein p65/RelA by the chlamydial protease-like activity factor (CPAF) impairs proinflammatory signaling in cells infected with Chlamydiae. J. Biol. Chem. 285:41320–27 [Google Scholar]
  28. Christian JG, Heymann J, Paschen SA, Vier J, Schauenburg L. 28.  et al. 2011. Targeting of a chlamydial protease impedes intracellular bacterial growth. PLOS Pathog. 7:e1002283 [Google Scholar]
  29. Clifton DR, Fields KA, Grieshaber SS, Dooley CA, Fischer ER. 29.  et al. 2004. A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin. PNAS 101:10166–71 [Google Scholar]
  30. da Cunha M, Milho C, Almeida F, Pais SV, Borges V. 30.  et al. 2014. Identification of type III secretion substrates of Chlamydia trachomatis using Yersinia enterocolitica as a heterologous system. BMC Microbiol. 14:40 [Google Scholar]
  31. De Clercq E, Kalmar I, Vanrompay D. 31.  2013. Animal models for studying female genital tract infection with Chlamydia trachomatis. Infect. Immun. 81:3060–67 [Google Scholar]
  32. Dean D, Bruno WJ, Wan R, Gomes JP, Devignot S. 32.  et al. 2009. Predicting phenotype and emerging strains among Chlamydia trachomatis infections. Emerg. Infect. Dis. 15:1385–94 [Google Scholar]
  33. DeMars R, Weinfurter J. 33.  2008. Interstrain gene transfer in Chlamydia trachomatis in vitro: mechanism and significance. J. Bacteriol. 190:1605–14 [Google Scholar]
  34. DeMars R, Weinfurter J, Guex E, Lin J, Potucek Y. 34.  2007. Lateral gene transfer in vitro in the intracellular pathogen Chlamydia trachomatis. J. Bacteriol. 189:991–1003 [Google Scholar]
  35. Dille S, Herbst K, Volceanov L, Nolke T, Kretz O, Hacker G. 35.  2014. Golgi fragmentation and sphingomyelin transport to Chlamydia trachomatis during penicillin-induced persistence do not depend on the cytosolic presence of the chlamydial protease CPAF. PLOS ONE 9:e103220 [Google Scholar]
  36. Ding H, Gong S, Tian Y, Yang Z, Brunham R, Zhong G. 36.  2013. Transformation of sexually transmitted infection-causing serovars of Chlamydia trachomatis using blasticidin for selection. PLOS ONE 8:e80534 [Google Scholar]
  37. Donati M, Huot-Creasy H, Humphrys M, Di Paolo M, Di Francesco A, Myers GS. 37.  2014. Genome sequence of Chlamydia suis MD56, isolated from the conjunctiva of a weaned piglet. Genome Announc. 2:e00425–14 [Google Scholar]
  38. Dutta T, Jain NK, McMillan NA, Parekh HS. 38.  2010. Dendrimer nanocarriers as versatile vectors in gene delivery. Nanomedicine 6:25–34 [Google Scholar]
  39. Falkow S. 39.  1988. Molecular Koch's postulates applied to microbial pathogenicity. Rev. Infect. Dis. 10:Suppl. 2S274–76 [Google Scholar]
  40. Farencena A, Comanducci M, Donati M, Ratti G, Cevenini R. 40.  1997. Characterization of a new isolate of Chlamydia trachomatis which lacks the common plasmid and has properties of biovar trachoma. Infect. Immun. 65:2965–69 [Google Scholar]
  41. Felsheim RF, Herron MJ, Nelson CM, Burkhardt NY, Barbet AF. 41.  et al. 2006. Transformation of Anaplasma phagocytophilum. BMC Biotechnol. 6:42 [Google Scholar]
  42. Fields KA, Fischer ER, Mead DJ, Hackstadt T. 42.  2005. Analysis of putative Chlamydia trachomatis chaperones Scc2 and Scc3 and their use in the identification of type III secretion substrates. J. Bacteriol. 187:6466–78 [Google Scholar]
  43. Fitch WM, Peterson EM, de la Maza LM. 43.  1993. Phylogenetic analysis of the outer-membrane-protein genes of Chlamydiae, and its implication for vaccine development. Mol. Biol. Evol. 10:892–913 [Google Scholar]
  44. Gérard HC, Mishra MK, Mao G, Wang S, Hali M. 44.  et al. 2013. Dendrimer-enabled DNA delivery and transformation of Chlamydia pneumoniae. Nanomedicine 9:996–1008 [Google Scholar]
  45. Gomes JP, Bruno WJ, Borrego MJ, Dean D. 45.  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. 186:4295–306 [Google Scholar]
  46. Gomes JP, Bruno WJ, Nunes A, Santos N, Florindo C. 46.  et al. 2007. Evolution of Chlamydia trachomatis diversity occurs by widespread interstrain recombination involving hotspots. Genome Res. 17:50–60 [Google Scholar]
  47. Gomes JP, Nunes A, Bruno WJ, Borrego MJ, Florindo C, Dean D. 47.  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. 188:275–86 [Google Scholar]
  48. Gong S, Yang Z, Lei L, Shen L, Zhong G. 48.  2013. Characterization of Chlamydia trachomatis plasmid-encoded open reading frames. J. Bacteriol. 195:3819–26 [Google Scholar]
  49. Harris SR, Clarke IN, Seth-Smith HM, Solomon AW, Cutcliffe LT. 49.  et al. 2012. Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nat. Genet. 44:413–19, S1 [Google Scholar]
  50. Hatch T. 50.  1996. Disulfide cross-linked envelope proteins: the functional equivalent of peptidoglycan in chlamydiae?. J. Bacteriol. 178:1–5 [Google Scholar]
  51. Hayes LJ, Yearsley P, Treharne JD, Ballard RA, Fehler GH, Ward ME. 51.  1994. Evidence for naturally occurring recombination in the gene encoding the major outer membrane protein of lymphogranuloma venereum isolates of Chlamydia trachomatis. Infect. Immun. 62:5659–63 [Google Scholar]
  52. Hobolt-Pedersen AS, Christiansen G, Timmerman E, Gevaert K, Birkelund S. 52.  2009. Identification of Chlamydia trachomatis CT621, a protein delivered through the type III secretion system to the host cell cytoplasm and nucleus. FEMS Immunol. Med. Microbiol. 57:46–58 [Google Scholar]
  53. Horn M. 53.  2008. Chlamydiae as symbionts in eukaryotes. Annu. Rev. Microbiol. 62:113–31 [Google Scholar]
  54. Hovis KM, Mojica S, McDermott JE, Pedersen L, Simhi C. 54.  et al. 2013. Genus-optimized strategy for the identification of chlamydial type III secretion substrates. Pathog. Dis. 69:213–22 [Google Scholar]
  55. Huang Y, Zhang Q, Yang Z, Conrad T, Liu Y, Zhong G. 55.  2015. Plasmid-encoded Pgp5 is a significant contributor to Chlamydia muridarum induction of hydrosalpinx. PLOS ONE 10:e0124840 [Google Scholar]
  56. Humphrys MS, Creasy T, Sun Y, Shetty AC, Chibucos MC. 56.  et al. 2013. Simultaneous transcriptional profiling of bacteria and their host cells. PLOS ONE 8:e80597 [Google Scholar]
  57. Hybiske K, Stephens RS. 57.  2007. Mechanisms of host cell exit by the intracellular bacterium Chlamydia. PNAS 104:11430–35 [Google Scholar]
  58. Jeffrey BM, Suchland RJ, Eriksen SG, Sandoz KM, Rockey DD. 58.  2013. Genomic and phenotypic characterization of in vitro-generated Chlamydia trachomatis recombinants. BMC Microbiol. 13:142 [Google Scholar]
  59. Jeffrey BM, Suchland RJ, Quinn KL, Davidson JR, Stamm WE, Rockey DD. 59.  2010. Genome sequencing of recent clinical Chlamydia trachomatis strains identifies loci associated with tissue tropism and regions of apparent recombination. Infect. Immun. 78:2544–53 [Google Scholar]
  60. Johnson CM, Fisher DJ. 60.  2013. Site-specific, insertional inactivation of incA in Chlamydia trachomatis using a group II intron. PLOS ONE 8:e83989 [Google Scholar]
  61. Johnson KA, Lee JK, Chen AL, Tan M, Sutterlin C. 61.  2015. Induction and inhibition of CPAF activity during analysis of Chlamydia-infected cells. Pathog. Dis. 73:1–8 [Google Scholar]
  62. Joseph SJ, Didelot X, Gandhi K, Dean D, Read TD. 62.  2011. Interplay of recombination and selection in the genomes of Chlamydia trachomatis. Biol. Dir. 6:28 [Google Scholar]
  63. Joseph SJ, Didelot X, Rothschild J, de Vries HJ, Morre SA. 63.  et al. 2012. Population genomics of Chlamydia trachomatis: insights on drift, selection, recombination, and population structure. Mol. Biol. Evol. 29:3933–46 [Google Scholar]
  64. Joseph SJ, Li B, Ghonasgi T, Haase CP, Qin ZS. 64.  et al. 2014. Direct amplification, sequencing and profiling of Chlamydia trachomatis strains in single and mixed infection clinical samples. PLOS ONE 9:e99290 [Google Scholar]
  65. Kalman S, Mitchell W, Marathe R, Lammel C, Fan J. 65.  et al. 1999. Comparative genomes of Chlamydia pneumoniae and C. trachomatis. Nat. Genet. 21:385–89 [Google Scholar]
  66. Kannan RM, Gerard HC, Mishra MK, Mao G, Wang S. 66.  et al. 2013. Dendrimer-enabled transformation of Chlamydia trachomatis. Microb. Pathog. 65:29–35 [Google Scholar]
  67. Kari L, Goheen MM, Randall LB, Taylor LD, Carlson JH. 67.  et al. 2011. Generation of targeted Chlamydia trachomatis null mutants. PNAS 108:7189–93 [Google Scholar]
  68. Kari L, Southern TR, Downey CJ, Watkins HS, Randall LB. 68.  et al. 2014. Chlamydia trachomatis polymorphic membrane protein D is a virulence factor involved in early host-cell interactions. Infect. Immun. 82:2756–62 [Google Scholar]
  69. Kari L, Whitmire WM, Olivares-Zavaleta N, Goheen MM, Taylor LD. 69.  et al. 2011. A live-attenuated chlamydial vaccine protects against trachoma in nonhuman primates. J. Exp. Med. 208:2217–23 [Google Scholar]
  70. Kokes M, Dunn JD, Granek JA, Nguyen BD, Barker JR. 70.  et al. 2015. Integrating chemical mutagenesis and whole-genome sequencing as a platform for forward and reverse genetic analysis of Chlamydia. Cell Host Microbe 17:716–25 [Google Scholar]
  71. Koo IC, Walthers D, Hefty PS, Kenney LJ, Stephens RS. 71.  2006. ChxR is a transcriptional activator in Chlamydia. PNAS 103:750–55 [Google Scholar]
  72. Lampe MF, Suchland RJ, Stamm WE. 72.  1993. Nucleotide sequence of the variable domains within the major outer membrane protein gene from serovariants of Chlamydia trachomatis. Infect. Immun. 61:213–19 [Google Scholar]
  73. Liu Y, Chen C, Gong S, Hou S, Qi M. 73.  et al. 2014. Transformation of Chlamydia muridarum reveals a role for Pgp5 in suppression of plasmid-dependent gene expression. J. Bacteriol. 196:989–98 [Google Scholar]
  74. Liu Y, Huang Y, Yang Z, Sun Y, Gong S. 74.  et al. 2014. Plasmid-encoded Pgp3 is a major virulence factor for Chlamydia muridarum to induce hydrosalpinx in mice. Infect. Immun. 82:5327–35 [Google Scholar]
  75. Longbottom D, Coulter LJ. 75.  2003. Animal chlamydioses and zoonotic implications. J. Comp. Pathol. 128:217–44 [Google Scholar]
  76. Lowden NM, Yeruva L, Johnson CM, Bowlin AK, Fisher DJ. 76.  2015. Use of aminoglycoside 3′ adenyltransferase as a selection marker for Chlamydia trachomatis intron-mutagenesis and in vivo intron stability. BMC Res. Notes 8:570 [Google Scholar]
  77. Lugert R, Kuhns M, Polch T, Gross U. 77.  2004. Expression and localization of type III secretion-related proteins of Chlamydia pneumoniae. Med. Microbiol. Immunol. 193:163–71 [Google Scholar]
  78. Marsh JW, Wee BA, Tyndall JD, Lott WB, Bastidas RJ. 78.  et al. 2015. A Chlamydia trachomatis strain with a chemically generated amino acid substitution (P370L) in the cthtrA gene shows reduced elementary body production. BMC Microbiol. 15:194 [Google Scholar]
  79. Matsumoto A. 79.  1988. Structural characteristics of chlamydial bodies. Microbiology of Chlamydia AL Barron 21–45 Boca Raton, FL: CRC [Google Scholar]
  80. Matsumoto A, Izutsu H, Miyashita N, Ohuchi M. 80.  1998. Plaque formation by and plaque cloning of Chlamydia trachomatis biovar trachoma. J. Clin. Microbiol. 36:3013–19 [Google Scholar]
  81. Millman K, Black CM, Johnson RE, Stamm WE, Jones RB. 81.  et al. 2004. Population-based genetic and evolutionary analysis of Chlamydia trachomatis urogenital strain variation in the United States. J. Bacteriol. 186:2457–65 [Google Scholar]
  82. Millman KL, Tavare S, Dean D. 82.  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. 183:5997–6008 [Google Scholar]
  83. Mishra MK, Gerard HC, Whittum-Hudson JA, Hudson AP, Kannan RM. 83.  2012. Dendrimer-enabled modulation of gene expression in Chlamydia trachomatis. Mol. Pharm. 9:413–21 [Google Scholar]
  84. Mishra MK, Kotta K, Hali M, Wykes S, Gerard HC. 84.  et al. 2011. PAMAM dendrimer-azithromycin conjugate nanodevices for the treatment of Chlamydia trachomatis infections. Nanomedicine 7:935–44 [Google Scholar]
  85. Mojica S, Huot Creasy H, Daugherty S, Read TD, Kim T. 85.  et al. 2011. Genome sequence of the obligate intracellular animal pathogen Chlamydia pecorum E58. J. Bacteriol. 193:3690 [Google Scholar]
  86. Mueller KE, Fields KA. 86.  2015. Application of beta-lactamase reporter fusions as an indicator of effector protein secretion during infections with the obligate intracellular pathogen Chlamydia trachomatis. PLOS ONE 10:e0135295 [Google Scholar]
  87. Mueller KE, Wolf K, Fields KA. 87.  2016. Gene deletion by fluorescence-reported allelic exchange mutagenesis in Chlamydia trachomatis. mBio 7:e01817–15 [Google Scholar]
  88. Mylonas I. 88.  2012. Female genital Chlamydia trachomatis infection: Where are we heading?. Arch. Gynecol. Obstet. 285:1271–85 [Google Scholar]
  89. Nguyen BD, Valdivia RH. 89.  2012. Virulence determinants in the obligate intracellular pathogen Chlamydia trachomatis revealed by forward genetic approaches. PNAS 109:1263–68 [Google Scholar]
  90. Nicholson TL, Olinger L, Chong K, Schoolnik G, Stephens RS. 90.  2003. Global stage-specific gene regulation during the developmental cycle of Chlamydia trachomatis. J. Bacteriol. 185:3179–89 [Google Scholar]
  91. Niehus E, Cheng E, Tan M. 91.  2008. DNA supercoiling-dependent gene regulation in Chlamydia. J. Bacteriol. 190:6419–27 [Google Scholar]
  92. O'Connell CM, AbdelRahman YM, Green E, Darville HK, Saira K. 92.  et al. 2011. Toll-like receptor 2 activation by Chlamydia trachomatis is plasmid dependent, and plasmid-responsive chromosomal loci are coordinately regulated in response to glucose limitation by C. trachomatis but not by C. muridarum. Infect. Immun. 79:1044–56 [Google Scholar]
  93. O'Connell CM, Ingalls RR, Andrews CW Jr, Scurlock AM, Darville T. 93.  2007. Plasmid-deficient Chlamydia muridarum fail to induce immune pathology and protect against oviduct disease. J. Immunol. 179:4027–34 [Google Scholar]
  94. O'Connell CM, Nicks KM. 94.  2006. A plasmid-cured Chlamydia muridarum strain displays altered plaque morphology and reduced infectivity in cell culture. Microbiology 152:1601–7 [Google Scholar]
  95. Oleykowski CA, Bronson Mullins CR, Godwin AK, Yeung AT. 95.  1998. Mutation detection using a novel plant endonuclease. Nucleic Acids Res. 26:4597–602 [Google Scholar]
  96. Olivares-Zavaleta N, Whitmire W, Gardner D, Caldwell HD. 96.  2010. Immunization with the attenuated plasmidless Chlamydia trachomatis L2(25667R) strain provides partial protection in a murine model of female genitourinary tract infection. Vaccine 28:1454–62 [Google Scholar]
  97. Omsland A, Beare PA, Hill J, Cockrell DC, Howe D. 97.  et al. 2011. Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl. Environ. Microbiol. 77:3720–25 [Google Scholar]
  98. Omsland A, Cockrell DC, Howe D, Fischer ER, Virtaneva K. 98.  et al. 2009. Host cell-free growth of the Q fever bacterium Coxiella burnetii. PNAS 106:4430–34 [Google Scholar]
  99. Omsland A, Sager J, Nair V, Sturdevant DE, Hackstadt T. 99.  2012. Developmental stage-specific metabolic and transcriptional activity of Chlamydia trachomatis in an axenic medium. PNAS 109:19781–85 [Google Scholar]
  100. Omsland A, Sixt BS, Horn M, Hackstadt T. 100.  2014. Chlamydial metabolism revisited: interspecies metabolic variability and developmental stage-specific physiologic activities. FEMS Microbiol. Rev. 38:779–801 [Google Scholar]
  101. Pais SV, Milho C, Almeida F, Mota LJ. 101.  2013. Identification of novel type III secretion chaperone-substrate complexes of Chlamydia trachomatis. PLOS ONE 8:e56292 [Google Scholar]
  102. Pannekoek Y, Morelli G, Kusecek B, Morre SA, Ossewaarde JM. 102.  et al. 2008. Multi locus sequence typing of Chlamydiales: clonal groupings within the obligate intracellular bacteria Chlamydia trachomatis. BMC Microbiol. 8:42 [Google Scholar]
  103. Peterson EM, Markoff BA, Schachter J, de la Maza LM. 103.  1990. The 7.5-kb plasmid present in Chlamydia trachomatis is not essential for the growth of this microorganism. Plasmid 23:144–48 [Google Scholar]
  104. Pirbhai M, Dong F, Zhong Y, Pan KZ, Zhong G. 104.  2006. The secreted protease factor CPAF is responsible for degrading pro-apoptotic BH3-only proteins in Chlamydia trachomatis-infected cells. J. Biol. Chem. 281:31495–501 [Google Scholar]
  105. Qin A, Tucker AM, Hines A, Wood DO. 105.  2004. Transposon mutagenesis of the obligate intracellular pathogen Rickettsia prowazekii. Appl. Environ. Microbiol. 70:2816–22 [Google Scholar]
  106. Qu Y, Frazer LC, O'Connell CM, Tarantal AF, Andrews CW Jr.. 106.  et al. 2015. Comparable genital tract infection, pathology, and immunity in rhesus macaques inoculated with wild-type or plasmid-deficient Chlamydia trachomatis serovar D. Infect. Immun. 83:4056–67 [Google Scholar]
  107. Rajaram K, Giebel AM, Toh E, Hu S, Newman JH. 107.  et al. 2015. Mutational analysis of the Chlamydia muridarum plasticity zone. Infect. Immun. 83:2870–81 [Google Scholar]
  108. Ramsey KH, Schripsema JH, Smith BJ, Wang Y, Jham BC. 108.  et al. 2014. Plasmid CDS5 influences infectivity and virulence in a mouse model of Chlamydia trachomatis urogenital infection. Infect. Immun. 82:3341–49 [Google Scholar]
  109. Read TD, Brunham RC, Shen C, Gill SR, Heidelberg JF. 109.  et al. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:1397–406 [Google Scholar]
  110. Read TD, Myers GS, Brunham RC, Nelson WC, Paulsen IT. 110.  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. 31:2134–47 [Google Scholar]
  111. Rockey DD. 111.  2011. Unraveling the basic biology and clinical significance of the chlamydial plasmid. J. Exp. Med. 208:2159–62 [Google Scholar]
  112. Rosario CJ, Hanson BR, Tan M. 112.  2014. The transcriptional repressor EUO regulates both subsets of Chlamydia late genes. Mol. Microbiol. 94:888–97 [Google Scholar]
  113. Rosario CJ, Tan M. 113.  2012. The early gene product EUO is a transcriptional repressor that selectively regulates promoters of Chlamydia late genes. Mol. Microbiol. 84:1097–107 [Google Scholar]
  114. Russell M, Darville T, Chandra-Kuntal K, Smith B, Andrews CW. O'Connell CM. 114.  Jr., 2011. Infectivity acts as in vivo selection for maintenance of the chlamydial cryptic plasmid. Infect. Immun. 79:98–107 [Google Scholar]
  115. Samudrala R, Heffron F, McDermott JE. 115.  2009. Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type III secretion systems. PLOS Pathog. 5:e1000375 [Google Scholar]
  116. Sega GA. 116.  1984. A review of the genetic effects of ethyl methanesulfonate. Mutat. Res. 134:113–42 [Google Scholar]
  117. Shaw AC, Vandahl BB, Larsen MR, Roepstorff P, Gevaert K. 117.  et al. 2002. Characterization of a secreted Chlamydia protease. Cell Microbiol. 4:411–24 [Google Scholar]
  118. Sliwa-Dominiak J, Suszynska E, Pawlikowska M, Deptula W. 118.  2013. Chlamydia bacteriophages. Arch. Microbiol. 195:765–71 [Google Scholar]
  119. Snavely EA, Kokes M, Dunn JD, Saka HA, Nguyen BD. 119.  et al. 2014. Reassessing the role of the secreted protease CPAF in Chlamydia trachomatis infection through genetic approaches. Pathog. Dis. 71:336–51 [Google Scholar]
  120. Somboonna N, Wan R, Ojcius DM, Pettengill MA, Joseph SJ. 120.  et al. 2011. Hypervirulent Chlamydia trachomatis clinical strain is a recombinant between lymphogranuloma venereum (L2) and D lineages. mBio 2:e00045–11 [Google Scholar]
  121. Song L, Carlson JH, Whitmire WM, Kari L, Virtaneva K. 121.  et al. 2013. Chlamydia trachomatis plasmid-encoded Pgp4 is a transcriptional regulator of virulence-associated genes. Infect. Immun. 81:636–44 [Google Scholar]
  122. Song L, Carlson JH, Zhou B, Virtaneva K, Whitmire WM. 122.  et al. 2014. Plasmid-mediated transformation tropism of chlamydial biovars. Pathog. Dis. 70:189–93 [Google Scholar]
  123. Stephens RS, Kalman S, Lammel C, Fan J, Marathe R. 123.  et al. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754–59 [Google Scholar]
  124. Stothard DR, Williams JA, Van Der Pol B, Jones RB. 124.  1998. Identification of a Chlamydia trachomatis serovar E urogenital isolate which lacks the cryptic plasmid. Infect. Immun. 66:6010–13 [Google Scholar]
  125. Subtil A, Delevoye C, Balana ME, Tastevin L, Perrinet S, Dautry-Varsat A. 125.  2005. A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates. Mol. Microbiol. 56:1636–47 [Google Scholar]
  126. Subtil A, Parsot C, Dautry-Varsat A. 126.  2001. Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery. Mol. Microbiol. 39:792–800 [Google Scholar]
  127. Suchland RJ, Sandoz KM, Jeffrey BM, Stamm WE, Rockey DD. 127.  2009. Horizontal transfer of tetracycline resistance among Chlamydia spp. in vitro. Antimicrob. Agents Chemother. 53:4604–11 [Google Scholar]
  128. Tam JE, Davis CH, Wyrick PB. 128.  1994. Expression of recombinant DNA introduced into Chlamydia trachomatis by electroporation. Can. J. Microbiol. 40:583–91 [Google Scholar]
  129. Tamura A, Matsumoto A, Higashi N. 129.  1967. Purification and chemical composition of reticulate bodies of the meningopneumonitis organisms. J. Bacteriol. 93:2003–8 [Google Scholar]
  130. Taylor HR, Burton MJ, Haddad D, West S, Wright H. 130.  2014. Trachoma. Lancet 384:2142–52 [Google Scholar]
  131. Thompson CC, Griffiths C, Nicod SS, Lowden NM, Wigneshweraraj S. 131.  et al. 2015. The Rsb phosphoregulatory network controls availability of the primary sigma factor in Chlamydia trachomatis and influences the kinetics of growth and development. PLOS Pathog. 11:e1005125 [Google Scholar]
  132. Thomson NR, Holden MT, Carder C, Lennard N, Lockey SJ. 132.  et al. 2008. Chlamydia trachomatis: Genome sequence analysis of lymphogranuloma venereum isolates. Genome Res. 18:161–71 [Google Scholar]
  133. Thomson NR, Yeats C, Bell K, Holden MT, Bentley SD. 133.  et al. 2005. The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. Genome Res. 15:629–40 [Google Scholar]
  134. Vandahl BB, Stensballe A, Roepstorff P, Christiansen G, Birkelund S. 134.  2005. Secretion of Cpn0796 from Chlamydia pneumoniae into the host cell cytoplasm by an autotransporter mechanism. Cell Microbiol. 7:825–36 [Google Scholar]
  135. Voigt A, Schofl G, Saluz HP. 135.  2012. The Chlamydia psittaci genome: a comparative analysis of intracellular pathogens. PLOS ONE 7:e35097 [Google Scholar]
  136. Vromman F, Laverriere M, Perrinet S, Dufour A, Subtil A. 136.  2014. Quantitative monitoring of the Chlamydia trachomatis developmental cycle using GFP-expressing bacteria, microscopy and flow cytometry. PLOS ONE 9:e99197 [Google Scholar]
  137. Wang X, Schwarzer C, Hybiske K, Machen TE, Stephens RS. 137.  2014. Developmental stage oxidoreductive states of Chlamydia and infected host cells. mBio 5:e01924 [Google Scholar]
  138. Wang Y, Cutcliffe LT, Skilton RJ, Persson K, Bjartling C, Clarke IN. 138.  2013. Transformation of a plasmid-free, genital tract isolate of Chlamydia trachomatis with a plasmid vector carrying a deletion in CDS6 revealed that this gene regulates inclusion phenotype. Pathog. Dis. 67:100–3 [Google Scholar]
  139. Wang Y, Cutcliffe LT, Skilton RJ, Ramsey KH, Thomson NR, Clarke IN. 139.  2014. The genetic basis of plasmid tropism between Chlamydia trachomatis and Chlamydia muridarum. Pathog. Dis. 72:19–23 [Google Scholar]
  140. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR, Clarke IN. 140.  2011. Development of a transformation system for Chlamydia trachomatis: restoration of glycogen biosynthesis by acquisition of a plasmid shuttle vector. PLOS Pathog. 7:e1002258 [Google Scholar]
  141. Wang Y, Kahane S, Cutcliffe LT, Skilton RJ, Lambden PR. 141.  et al. 2013. Genetic transformation of a clinical (genital tract), plasmid-free isolate of Chlamydia trachomatis: engineering the plasmid as a cloning vector. PLOS ONE 8:e59195 [Google Scholar]
  142. Weber MM, Bauler LD, Lam J, Hackstadt T. 142.  2015. Expression and localization of predicted inclusion membrane proteins in Chlamydia trachomatis. Infect. Immun. 83:4710–18 [Google Scholar]
  143. Wickstrum J, Sammons LR, Restivo KN, Hefty PS. 143.  2013. Conditional gene expression in Chlamydia trachomatis using the Tet system. PLOS ONE 8:e76743 [Google Scholar]
  144. 144. World Health Organ 2012. Global Incidence and Prevalence of Selected Curable Sexually Transmitted Infections—2008 Geneva: World Health Inst. [Google Scholar]
  145. 145. World Health Organ 2015. Trachoma. Fact sheet 382, World Health Organ., Geneva. http://www.who.int/mediacentre/factsheets/fs382/en/ [Google Scholar]
  146. Xu S, Battaglia L, Bao X, Fan H. 146.  2013. Chloramphenicol acetyltransferase as a selection marker for chlamydial transformation. BMC Res. Notes 6:377 [Google Scholar]
  147. Yang C, Starr T, Song L, Carlson JH, Sturdevant GL. 147.  et al. 2015. Chlamydial lytic exit from host cells is plasmid regulated. mBio 6:e01648–15 [Google Scholar]
  148. Yang CL, Maclean I, Brunham RC. 148.  1993. DNA sequence polymorphism of the Chlamydia trachomatis omp1 gene. J. Infect. Dis. 168:1225–30 [Google Scholar]
  149. Yu HH, Kibler D, Tan M. 149.  2006. In silico prediction and functional validation of σ28-regulated genes in Chlamydia and Escherichia coli. J. Bacteriol. 188:8206–12 [Google Scholar]
  150. Zhong G. 150.  2009. Killing me softly: chlamydial use of proteolysis for evading host defenses. Trends Microbiol. 17:467–74 [Google Scholar]
  151. Zhong G, Fan P, Ji H, Dong F, Huang Y. 151.  2001. Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors.. J. Exp. Med. 193:935–42 [Google Scholar]
/content/journals/10.1146/annurev-micro-102215-095539
Loading
/content/journals/10.1146/annurev-micro-102215-095539
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error