Home LiteratureArticle Details
PMID: 12682364 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae.

Nucleic acids research ·Vol. 31 ·No. 8 ·2003-04-15 ·Pages 2134-47

Read TD, Myers GS, Brunham RC, Nelson WC, Paulsen IT, Heidelberg J, Holtzapple E, Khouri H, Federova NB, Carty HA, Umayam LA, Haft DH, Peterson J, Beanan MJ, White O, Salzberg SL, Hsia RC, McClarty G, Rank RG, Bavoil PM, Fraser CM

Abstract

The genome of Chlamydophila caviae (formerly Chlamydia psittaci, GPIC isolate) (1 173 390 nt with a plasmid of 7966 nt) was determined, representing the fourth species with a complete genome sequence from the Chlamydiaceae family of obligate intracellular bacterial pathogens. Of 1009 annotated genes, 798 were conserved in all three other completed Chlamydiaceae genomes. The C.caviae genome contains 68 genes that lack orthologs in any other completed chlamydial genomes, including tryptophan and thiamine biosynthesis determinants and a ribose-phosphate pyrophosphokinase, the product of the prsA gene. Notable amongst these was a novel member of the virulence-associated invasin/intimin family (IIF) of Gram-negative bacteria. Intriguingly, two authentic frameshift mutations in the ORF indicate that this gene is not functional. Many of the unique genes are found in the replication termination region (RTR or plasticity zone), an area of frequent symmetrical inversion events around the replication terminus shown to be a hotspot for genome variation in previous genome sequencing studies. In C.caviae, the RTR includes several loci of particular interest including a large toxin gene and evidence of ancestral insertion(s) of a bacteriophage. This toxin gene, not present in Chlamydia pneumoniae, is a member of the YopT effector family of type III-secreted cysteine proteases. One gene cluster (guaBA-add) in the RTR is much more similar to orthologs in Chlamydia muridarum than those in the phylogenetically closest species C.pneumoniae, suggesting the possibility of horizontal transfer of genes between the rodent-associated Chlamydiae. With most genes observed in the other chlamydial genomes represented, C.caviae provides a good model for the Chlamydiaceae and a point of comparison against the human atherosclerosis-associated C.pneumoniae. This crucial addition to the set of completed Chlamydiaceae genome sequences is enabling dissection of the roles played by niche-specific genes in these important bacterial pathogens.

MeSH Terms
Adhesins, Bacterial/genetics Amino Acid Sequence Carrier Proteins/genetics Chlamydiaceae/genetics Chlamydophila psittaci/genetics Chromosomes, Bacterial/genetics DNA, Bacterial/chemistry,genetics Escherichia coli Proteins Evolution, Molecular Genome, Bacterial Molecular Sequence Data Plasmids/genetics Sequence Analysis, DNA Sequence Homology, Amino Acid Virulence/genetics
Chemicals
Adhesins, Bacterial Carrier Proteins DNA, Bacterial Escherichia coli Proteins invasin, Yersinia eaeA protein, E coli
Authors & Affiliations
21 authors, click to expand affiliations / ORCID
Read T D
The Institute for Genomic Research, 9712 Medical Center Drive, Rockville, MD 20850, USA. [email protected]
Myers G S A
Brunham R C
Nelson W C
Paulsen I T
Heidelberg J
Holtzapple E
Khouri H
Federova N B
Carty H A
Umayam L A
Haft D H
Peterson J
Beanan M J
White O
Salzberg S L
Hsia R-c
McClarty G
Rank R G
Bavoil P M
Fraser C M
References (69)
69 references, click to expand
  1. Microviridae, a family divided: isolation, characterization, and genome sequence of phiMH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus.
    J Bacteriol. 2002 Feb;184(4):1089-94 PMID: 11807069
  2. Chlamydia pneumoniae as a respiratory pathogen.
    Front Biosci. 2002 Mar 1;7:e66-76 PMID: 11861211
  3. Microbial minimalism: genome reduction in bacterial pathogens.
    Cell. 2002 Mar 8;108(5):583-6 PMID: 11893328
  4. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis.
    Cell. 2002 May 31;109(5):575-88 PMID: 12062101
  5. Chlamydia trachomatis induces remodeling of the actin cytoskeleton during attachment and entry into HeLa cells.
    Infect Immun. 2002 Jul;70(7):3793-803 PMID: 12065523
  6. Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells.
    Cell Microbiol. 2002 Jul;4(7):447-60 PMID: 12102690
  7. The Pfam protein families database.
    Nucleic Acids Res. 2002 Jan 1;30(1):276-80 PMID: 11752314
  8. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi.
    Nature. 1997 Dec 11;390(6660):580-6 PMID: 9403685
  9. Microbial gene identification using interpolated Markov models.
    Nucleic Acids Res. 1998 Jan 15;26(2):544-8 PMID: 9421513
  10. Type III secretion in Chlamydia: a case of déjà vu?
    Mol Microbiol. 1998 May;28(4):860-2 PMID: 9643553
  11. Isolation and characterization of toluene-sensitive mutants from the toluene-resistant bacterium Pseudomonas putida GM73.
    J Bacteriol. 1998 Jul;180(14):3692-6 PMID: 9658016
  12. A common motif of eukaryotic glycosyltransferases is essential for the enzyme activity of large clostridial cytotoxins.
    J Biol Chem. 1998 Jul 31;273(31):19566-72 PMID: 9677381
  13. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells.
    Mol Microbiol. 1998 Aug;29(3):915-29 PMID: 9723929
  14. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis.
    Science. 1998 Oct 23;282(5389):754-9 PMID: 9784136
  15. Chlamydia: old ideas crushed, new mysteries bared.
    Science. 1998 Oct 23;282(5389):638-9 PMID: 9841415
  16. Chlamydia pneumoniae and cardiovascular disease.
    Emerg Infect Dis. 1998 Oct-Dec;4(4):571-9 PMID: 9866733
  17. Comparative genomes of Chlamydia pneumoniae and C. trachomatis.
    Nat Genet. 1999 Apr;21(4):385-9 PMID: 10192388
  18. 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. 1999 Apr;49 Pt 2:415-40 PMID: 10319462
  19. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima.
    Nature. 1999 May 27;399(6734):323-9 PMID: 10360571
  20. Molecular basis defining human Chlamydia trachomatis tissue tropism. A possible role for tryptophan synthase.
    J Biol Chem. 2002 Jul 26;277(30):26893-903 PMID: 12011099
  21. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells.
    Cell. 1987 Aug 28;50(5):769-78 PMID: 3304658
  22. Two distinct forms of Chlamydia psittaci associated with disease and infertility in Phascolarctos cinereus (koala).
    Infect Immun. 1988 Aug;56(8):1897-900 PMID: 3397180
  23. Further characterization of a bacteriophage recovered from an avian strain of Chlamydia psittaci.
    J Gen Virol. 1989 Jun;70 ( Pt 6):1321-7 PMID: 2732718
  24. Analysis of the complete nucleotide sequence of Chp1, a phage which infects avian Chlamydia psittaci.
    J Gen Virol. 1989 Dec;70 ( Pt 12):3381-90 PMID: 2607341
  25. Partial characterization of an 89-kDa highly immunoreactive protein from Chlamydia psittaci A/22 causing ovine abortion.
    FEMS Microbiol Lett. 1991 Jun 1;65(1):111-5 PMID: 1714846
  26. Pathogenesis of endometritis and salpingitis in a guinea pig model of chlamydial genital infection.
    Am J Pathol. 1992 Apr;140(4):927-36 PMID: 1562052
  27. Chlamydia pneumoniae, strain TWAR pneumonia.
    Annu Rev Med. 1992;43:317-23 PMID: 1580592
  28. Chlamydia pecorum--the fourth species of genus Chlamydia.
    Microbiol Immunol. 1993;37(7):516-22 PMID: 8231966
  29. Expression of recombinant DNA introduced into Chlamydia trachomatis by electroporation.
    Can J Microbiol. 1994 Jul;40(7):583-91 PMID: 8076253
  30. Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species.
    Cell. 1995 Feb 10;80(3):507-15 PMID: 7859291
  31. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd.
    Science. 1995 Jul 28;269(5223):496-512 PMID: 7542800
  32. The minimal gene complement of Mycoplasma genitalium.
    Science. 1995 Oct 20;270(5235):397-403 PMID: 7569993
  33. Molecular characterization of a carboxy-terminal eukaryotic-cell-binding domain of intimin from enteropathogenic Escherichia coli.
    Infect Immun. 1995 Nov;63(11):4323-8 PMID: 7591066
  34. Chlamydia pneumoniae (TWAR).
    Clin Microbiol Rev. 1995 Oct;8(4):451-61 PMID: 8665464
  35. Asymmetric substitution patterns in the two DNA strands of bacteria.
    Mol Biol Evol. 1996 May;13(5):660-5 PMID: 8676740
  36. Psittacosis.
    Semin Respir Infect. 1997 Mar;12(1):7-11 PMID: 9097370
  37. Type III secretion genes identify a putative virulence locus of Chlamydia.
    Mol Microbiol. 1997 Jul;25(2):351-9 PMID: 9282747
  38. Coiled-coil domains in proteins secreted by type III secretion systems.
    Mol Microbiol. 1997 Jul;25(2):423-5 PMID: 9282753
  39. A genomic perspective on protein families.
    Science. 1997 Oct 24;278(5338):631-7 PMID: 9381173
  40. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells.
    Cell. 1997 Nov 14;91(4):511-20 PMID: 9390560
  41. Epidemiology of Chlamydia pneumoniae in atherosclerosis.
    Am Heart J. 1999 Nov;138(5 Pt 2):S500-3 PMID: 10539858
  42. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39.
    Nucleic Acids Res. 2000 Mar 15;28(6):1397-406 PMID: 10684935
  43. Molecular characterization of a bacteriophage (Chp2) from Chlamydia psittaci.
    J Virol. 2000 Apr;74(8):3464-9 PMID: 10729119
  44. Involvement of a conserved tryptophan residue in the UDP-glucose binding of large clostridial cytotoxin glycosyltransferases.
    J Biol Chem. 2000 May 5;275(18):13228-34 PMID: 10788427
  45. Comparison of whole genome sequences of Chlamydia pneumoniae J138 from Japan and CWL029 from USA.
    Nucleic Acids Res. 2000 Jun 15;28(12):2311-4 PMID: 10871362
  46. Microvirus of chlamydia psittaci strain guinea pig inclusion conjunctivitis: isolation and molecular characterization.
    Microbiology. 2000 Jul;146 ( Pt 7):1651-60 PMID: 10878129
  47. Chlamydia pneumoniae and the risk of first ischemic stroke : The Northern Manhattan Stroke Study.
    Stroke. 2000 Jul;31(7):1521-5 PMID: 10884447
  48. Exploitation of host cells by enteropathogenic Escherichia coli.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8799-806 PMID: 10922038
  49. Bacterial toxins modifying the actin cytoskeleton.
    Int Microbiol. 1999 Sep;2(3):185-94 PMID: 10943412
  50. Phage infection of the obligate intracellular bacterium, Chlamydia psittaci strain guinea pig inclusion conjunctivitis.
    Microbes Infect. 2000 Jun;2(7):761-72 PMID: 10955956
  51. Signaling and invasin-promoted uptake via integrin receptors.
    Microbes Infect. 2000 Jun;2(7):793-801 PMID: 10955960
  52. Genome sequencing and our understanding of chlamydiae.
    Infect Immun. 2000 Oct;68(10):5473-9 PMID: 10992442
  53. Association of Chlamydia pneumoniae immunoglobulin A seropositivity and risk of lung cancer.
    Cancer Epidemiol Biomarkers Prev. 2000 Nov;9(11):1263-6 PMID: 11097237
  54. Evidence for the secretion of Chlamydia trachomatis CopN by a type III secretion mechanism.
    Mol Microbiol. 2000 Dec;38(5):1048-60 PMID: 11123678
  55. Identification and characterization of BipA, a Bordetella Bvg-intermediate phase protein.
    Mol Microbiol. 2001 Jan;39(1):65-78 PMID: 11123689
  56. CD8+ T cells recognize an inclusion membrane-associated protein from the vacuolar pathogen Chlamydia trachomatis.
    Proc Natl Acad Sci U S A. 2001 Jan 30;98(3):1160-5 PMID: 11158611
  57. Evolution of prokaryotic gene order: genome rearrangements in closely related species.
    Trends Genet. 2001 Jan;17(1):10-3 PMID: 11163906
  58. Evidence for symmetric chromosomal inversions around the replication origin in bacteria.
    Genome Biol. 2000;1(6):RESEARCH0011 PMID: 11178265
  59. Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review.
    Clin Microbiol Rev. 2001 Apr;14(2):336-63 PMID: 11292642
  60. Bap, a Staphylococcus aureus surface protein involved in biofilm formation.
    J Bacteriol. 2001 May;183(9):2888-96 PMID: 11292810
  61. Pseudogenes, junk DNA, and the dynamics of Rickettsia genomes.
    Mol Biol Evol. 2001 May;18(5):829-39 PMID: 11319266
  62. Comparative analysis of Chlamydia bacteriophages reveals variation localized to a putative receptor binding domain.
    Microb Comp Genomics. 2000;5(4):223-31 PMID: 11471835
  63. Characterization of a hypervariable region in the genome of Chlamydophila pneumoniae.
    FEMS Microbiol Lett. 2001 Sep 25;203(2):241-8 PMID: 11583855
  64. Deletional bias and the evolution of bacterial genomes.
    Trends Genet. 2001 Oct;17(10):589-96 PMID: 11585665
  65. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18.
    Nature. 2001 Oct 25;413(6858):848-52 PMID: 11677608
  66. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2.
    Nature. 2001 Oct 25;413(6858):852-6 PMID: 11677609
  67. Chlamydia trachomatis cytotoxicity associated with complete and partial cytotoxin genes.
    Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13984-9 PMID: 11707582
  68. Polymorphic proteins of Chlamydia spp.--autotransporters beyond the Proteobacteria.
    Trends Microbiol. 2001 Dec;9(12):573-8 PMID: 11728862
  69. Genomic approach for analysis of surface proteins in Chlamydia pneumoniae.
    Infect Immun. 2002 Jan;70(1):368-79 PMID: 11748203
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2003-04-15
Pages
2134-47
Language
English
Region
England
NLM ID
0411011
PMCID
PMC153749
Subset
IM
Grants
NIAID NIH HHS · AI43359 · United States
Databases
GENBANK
AE015925, AE015926
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]