is an obligate intracellular bacterium that can cause significant disease among a broad range of hosts. In humans, this organism may cause psittacosis, a respiratory disease that can spread to involve multiple organs, and in rare untreated cases may be fatal. There are ten known genotypes based on sequencing the major outer-membrane protein gene, , of Each genotype has overlapping host preferences and virulence characteristics. Recent studies have compared among other members of the family and showed that this species frequently switches hosts and has undergone multiple genomic rearrangements. In this study, we sequenced five genomes of strains representing four genotypes, A, B, D and E. Due to the known association of the type III secretion system (T3SS) and polymorphic outer-membrane proteins (Pmps) with host tropism and virulence potential, we performed a comparative analysis of these elements among these five strains along with a representative genome from each of the remaining six genotypes previously sequenced. We found significant genetic variation in the Pmps and tbl3SS genes that may partially explain differences noted in host infection and disease.


Article metrics loading...

Loading full text...

Full text loading...



  1. Abdelrahman Y.M., Belland R.J. (2005). The chlamydial developmental cycleFEMS Microbiol Rev 29949959 [View Article][PubMed]. [Google Scholar]
  2. Alikhan N.F., Petty N.K., Ben Zakour N.L., Beatson S.A. (2011). blast Ring Image Generator (brig): simple prokaryote genome comparisonsBMC Genomics 12402412 [View Article][PubMed]. [Google Scholar]
  3. Assefa S., Keane T.M., Otto T.D., Newbold C., Berriman M. (2009). abacas: algorithm-based automatic contiguation of assembled sequencesBioinformatics 2519681969 [View Article][PubMed]. [Google Scholar]
  4. Beeckman D.S.A., Vanrompay D.C.G. (2009). Zoonotic Chlamydophila psittaci infections from a clinical perspectiveClin Microbiol Infect 151117 [View Article][PubMed]. [Google Scholar]
  5. Beeckman D.S.A., Vanrompay D.C.G. (2010). Biology and intracellular pathogenesis of high or low virulent Chlamydophila psittaci strains in chicken macrophagesVet Microbiol 141342353 [View Article][PubMed]. [Google Scholar]
  6. Betts H.J., Twiggs L.E., Sal M.S., Wyrick P.B., Fields K.A. (2008). Bioinformatic and biochemical evidence for the identification of the type III secretion system needle protein of Chlamydia trachomatis J Bacteriol 19016801690 [View Article][PubMed]. [Google Scholar]
  7. Darling A.E., Mau B., Perna N.T. (2010). progressiveMauve: multiple genome alignment with gene gain, loss and rearrangementPLoS One 5e11147 [View Article][PubMed]. [Google Scholar]
  8. Davis D.J. (1949). The use of phenolized allantoic fluid antigen in the complement fixation test for psittacosisJ Immunol 62193200[PubMed]. [Google Scholar]
  9. Fields K.A., Mead D.J., Dooley C.A., Hackstadt T. (2003). Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle developmentMol Microbiol 48671683 [View Article][PubMed]. [Google Scholar]
  10. Francis T., Magill T.P. (1938). An unidentified virus producing acute meningitis and pneumonitis in experimental animalsJ Exp Med 68147160 [View Article][PubMed]. [Google Scholar]
  11. Gaede W., Reckling K.F., Dresenkamp B., Kenklies S., Schubert E., Noack U., Irmscher H.M., Ludwig C., Hotzel H., Sachse K. (2008). Chlamydophila psittaci infections in humans during an outbreak of psittacosis from poultry in GermanyZoonoses Public Health 55184188 [View Article][PubMed]. [Google Scholar]
  12. Gardner S.N., Hall B.G. (2013). When whole-genome alignments just won't work: kSNP v2 software for alignment-free SNP discovery and phylogenetics of hundreds of microbial genomesPLoS One 8e81760 [View Article][PubMed]. [Google Scholar]
  13. Haag-Wackernagel D., Moch H. (2004). Health hazards posed by feral pigeonsJ Infect 48307313 [View Article][PubMed]. [Google Scholar]
  14. Harkinezhad T., Verminnen K., Van Droogenbroeck C., Vanrompay D. (2007). Chlamydophila psittaci genotype E/B transmission from African grey parrots to humansJ Med Microbiol 5610971100 [View Article][PubMed]. [Google Scholar]
  15. Harkinezhad T., Geens T., Vanrompay D. (2009). Chlamydophila psittaci infections in birds: a review with emphasis on zoonotic consequencesVet Microbiol 1356877 [View Article][PubMed]. [Google Scholar]
  16. Heddema E.R., Ter Sluis S., Buys J.A., Vandenbroucke-Grauls C.M.J.E., van Wijnen J.H., Visser C.E. (2006a). Prevalence of Chlamydophila psittaci in fecal droppings from feral pigeons in Amsterdam, The NetherlandsAppl Environ Microbiol 7244234425 [View Article][PubMed]. [Google Scholar]
  17. Heddema E.R., van Hannen E.J., Duim B., de Jongh B.M., Kaan J.A., van Kessel R., Lumeij J.T., Visser C.E., Vandenbroucke-Grauls C.M.J.E. (2006b). An outbreak of psittacosis due to Chlamydophila psittaci genotype A in a veterinary teaching hospitalJ Med Microbiol 5515711575 [View Article][PubMed]. [Google Scholar]
  18. Heddema E.R., van Hannen E.J., Duim B., Vandenbroucke-Grauls C.M.J.E., Pannekoek Y. (2006c). Genotyping of Chlamydophila psittaci in human samplesEmerg Infect Dis 1219891990 [View Article][PubMed]. [Google Scholar]
  19. Herrmann M., Schuhmacher A., Mühldorfer I., Melchers K., Prothmann C., Dammeier S. (2006). Identification and characterization of secreted effector proteins of Chlamydophila pneumoniae TW183Res Microbiol 157513524 [View Article][PubMed]. [Google Scholar]
  20. Hotzel H., Berndt A., Melzer F., Sachse K. (2004). Occurrence of Chlamydiaceae spp. in a wild boar (Sus scrofa L.) population in Thuringia (Germany)Vet Microbiol 103121126 [View Article][PubMed]. [Google Scholar]
  21. Hsia R.C., Pannekoek Y., Ingerowski E., Bavoil P.M. (1997). Type III secretion genes identify a putative virulence locus of Chlamydia Mol Microbiol 25351359 [View Article][PubMed]. [Google Scholar]
  22. Hueck C.J. (1998). Type III protein secretion systems in bacterial pathogens of animals and plantsMicrobiol Mol Biol Rev 62379433[PubMed]. [Google Scholar]
  23. Hunter S., Jones P., Mitchell A., Apweiler R., Attwood T.K., Bateman A., Bernard T., Binns D., Bork P., other authors. (2012). InterPro in 2011: new developments in the family and domain prediction databaseNucleic Acids Res 40(D1), D306D312 [View Article][PubMed]. [Google Scholar]
  24. Jones P., Binns D., Chang H.Y., Fraser M., Li W., McAnulla C., McWilliam H., Maslen J., Mitchell A., other authors. (2014). InterProScan 5: genome-scale protein function classificationBioinformatics 3012361240 [View Article][PubMed]. [Google Scholar]
  25. Kaleta E.F., Taday E.M.A. (2003). Avian host range of Chlamydophila spp. based on isolation, antigen detection and serologyAvian Pathol 32435461 [View Article][PubMed]. [Google Scholar]
  26. Kalman S., Mitchell W., Marathe R., Lammel C., Fan J., Hyman R.W., Olinger L., Grimwood J., Davis R.W., Stephens R.S. (1999). Comparative genomes of Chlamydia pneumoniae C. trachomatis Nat Genet 21385389 [View Article][PubMed]. [Google Scholar]
  27. Liechti G.W., Kuru E., Hall E., Kalinda A., Brun Y.V., VanNieuwenhze M., Maurelli A.T. (2014). A new metabolic cell-wall labelling method reveals peptidoglycan in Chlamydia trachomatis Nature 506507510 [View Article][PubMed]. [Google Scholar]
  28. Miller C.D., Songer J.R., Sullivan J.F. (1987). A twenty-five year review of laboratory-acquired human infections at the National Animal Disease CenterAm Ind Hyg Assoc J 48271275 [View Article][PubMed]. [Google Scholar]
  29. Mitchell S.L., Wolff B.J., Thacker W.L., Ciembor P.G., Gregory C.R., Everett K.D.E., Ritchie B.W., Winchell J.M. (2009). Genotyping of Chlamydophila psittaci by real-time PCR and high-resolution melt analysisJ Clin Microbiol 47175181 [View Article][PubMed]. [Google Scholar]
  30. Mota L.J., Cornelis G.R. (2005). The bacterial injection kit: type III secretion systemsAnn Med 37234249 [View Article][PubMed]. [Google Scholar]
  31. Mukhopadhyay S., Clark A.P., Sullivan E.D., Miller R.D., Summersgill J.T. (2004). Detailed protocol for purification of Chlamydia pneumoniae elementary bodiesJ Clin Microbiol 4232883290 [View Article][PubMed]. [Google Scholar]
  32. Muschiol S., Normark S., Henriques-Normark B., Subtil A. (2009). Small molecule inhibitors of the Yersinia type III secretion system impair the development of Chlamydia after entry into host cellsBMC Microbiol 975 [View Article][PubMed]. [Google Scholar]
  33. Neuwirth E. (2007 RColorBrewer: ColorBrewer palettes. R package version 1.0–2.
  34. Page L.A. (1966). Interspecies transfer of psittacosis-LGV-trachoma agents: pathogenicity of two avian and two mammalian strains for eight species of birds and mammalsAm J Vet Res 27397407[PubMed]. [Google Scholar]
  35. Pavelka M.S. Jr, Jacobs W.R. Jr (1996). Biosynthesis of diaminopimelate, the precursor of lysine and a component of peptidoglycan, is an essential function of Mycobacterium smegmatis J Bacteriol 17864966507[PubMed]. [Google Scholar]
  36. Peters J., Wilson D.P., Myers G., Timms P., Bavoil P.M. (2007). Type III secretion à la Chlamydia Trends Microbiol 15241251 [View Article][PubMed]. [Google Scholar]
  37. Read T.D., Brunham R.C., Shen C., Gill S.R., Heidelberg J.F., White O., Hickey E.K., Peterson J., Utterback T., other authors. (2000). Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39Nucleic Acids Res 2813971406 [View Article][PubMed]. [Google Scholar]
  38. Read T.D., Myers G.S.A., Brunham R.C., Nelson W.C., Paulsen I.T., Heidelberg J., Holtzapple E., Khouri H., Federova N.B., other authors. (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 3121342147 [View Article][PubMed]. [Google Scholar]
  39. Read T.D., Joseph S.J., Didelot X., Liang B., Patel L., Dean D. (2013). Comparative analysis of Chlamydia psittaci genomes reveals the recent emergence of a pathogenic lineage with a broad host rangeMBio 4e00604e00612 [View Article][PubMed]. [Google Scholar]
  40. Rockey D.D., Lenart J., Stephens R.S. (2000). Genome sequencing and our understanding of Chlamydiae Infect Immun 6854735479 [View Article][PubMed]. [Google Scholar]
  41. Rambaut A. (2015 FigTree. 1.4.2 ednhttp://tree.bio.ed.ac.uk/software/figtree/.
  42. Sievers F., Wilm A., Dineen D., Gibson T.J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M., other authors. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal OmegaMol Syst Biol 7539 [View Article][PubMed]. [Google Scholar]
  43. Smith K.A., Campbell C.T., Murphy J., Stobierski M.G., Tengelsen L.A. (2011). Compendium of Measures to Control Chlamydophila psittaci Infection Among Humans (Psittacosis) and Pet Birds (Avian Chlamydiosis), 2010 National Association of State Public Health Veterinarians (NASPHV)J Exot Pet Med 203245 [View Article]. [Google Scholar]
  44. Somboonna N., Wan R., Ojcius D.M., Pettengill M.A., Joseph S.J., Chang A., Hsu R., Read T.D., Dean D. (2011). Hypervirulent Chlamydia trachomatis clinical strain is a recombinant between lymphogranuloma venereum (L(2)) and D lineagesMBio 2e00045e11 [View Article][PubMed]. [Google Scholar]
  45. Stamatakis A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogeniesBioinformatics 3013121313 [View Article][PubMed]. [Google Scholar]
  46. Stephens R.S., Kalman S., Lammel C., Fan J., Marathe R., Aravind L., Mitchell W., Olinger L., Tatusov R.L., other authors. (1998). Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis Science 282754759 [View Article][PubMed]. [Google Scholar]
  47. Stone C.B., Johnson D.L., Bulir D.C., Gilchrist J.D., Mahony J.B. (2008). Characterization of the putative type III secretion ATPase CdsN (Cpn0707) of Chlamydophila pneumoniae J Bacteriol 19065806588 [View Article][PubMed]. [Google Scholar]
  48. Thomson N.R., Yeats C., Bell K., Holden M.T.G., Bentley S.D., Livingstone M., Cerdeño-Tárraga A.M., Harris B., Doggett J., other authors. (2005). The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variationGenome Res 15629640 [View Article][PubMed]. [Google Scholar]
  49. Valdivia R.H. (2008). Chlamydia effector proteins and new insights into chlamydial cellular microbiologyCurr Opin Microbiol 115359 [View Article][PubMed]. [Google Scholar]
  50. Van Lent S., Piet J.R., Beeckman D., van der Ende A., Van Nieuwerburgh F., Bavoil P., Myers G., Vanrompay D., Pannekoek Y. (2012). Full genome sequences of all nine Chlamydia psittaci genotype reference strainsJ Bacteriol 19469306931 [View Article][PubMed]. [Google Scholar]
  51. Voigt A., Schöfl G., Saluz H.P. (2012). The Chlamydia psittaci genome: a comparative analysis of intracellular pathogensPLoS One 7e35097 [View Article][PubMed]. [Google Scholar]
  52. Warnes G.R., Bolker B., Lumley T. (2014 Gplots: Various R programming tools for plotting data. R package version 2.6.0. .
  53. Wreghitt T.G., Taylor C.E.D. (1988). Incidence of respiratory tract chlamydial infections and importation of psittacine birdsLancet 331582 [View Article][PubMed]. [Google Scholar]

Data & Media loading...


Supplementary Data

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