BLAST screening of chlamydial genomes to identify signature proteins that are unique for the Chlamydiales, Chlamydiaceae, Chlamydophila and Chlamydia groups of species

BackgroundChlamydiae species are of much importance from a clinical viewpoint. Their diversity both in terms of their numbers as well as clinical involvement are presently believed to be significantly underestimated. The obligate intracellular nature of chlamydiae has also limited their genetic and biochemical studies. Thus, it is of importance to develop additional means for their identification and characterization.ResultsWe have carried out analyses of available chlamydiae genomes to identify sets of unique proteins that are either specific for all Chlamydiales genomes, or different Chlamydiaceae family members, or members of the Chlamydia and Chlamydophila genera, or those unique to Protochlamydia amoebophila, but which are not found in any other bacteria. In total, 59 Chlamydiales-specific proteins, 79 Chlamydiaceae-specific proteins, 20 proteins each that are specific for both Chlamydia and Chlamydophila and 445 ORFs that are Protochlamydia-specific were identified. Additionally, 33 cases of possible gene loss or lateral gene transfer were also detected.ConclusionThe identified chlamydiae-lineage specific proteins, many of which are highly conserved, provide novel biomarkers that should prove of much value in the diagnosis of these bacteria and in exploration of their prevalence and diversity. These conserved protein sequences (CPSs) also provide novel therapeutic targets for drugs that are specific for these bacteria. Lastly, functional studies on these chlamydiae or chlamydiae subgroup-specific proteins should lead to important insights into lineage-specific adaptations with regards to development, infectivity and pathogenicity.

[1]  M. W. Taylor,et al.  'Candidatus Protochlamydia amoebophila', an endosymbiont of Acanthamoeba spp. , 2005, International journal of systematic and evolutionary microbiology.

[2]  Dmitrij Frishman,et al.  Illuminating the Evolutionary History of Chlamydiae , 2004, Science.

[3]  K. Kousoulas,et al.  Structures of and allelic diversity and relationships among the major outer membrane protein (ompA) genes of the four chlamydial species , 1993, Journal of bacteriology.

[4]  W. Newhall Biosynthesis and disulfide cross-linking of outer membrane components during the growth cycle of Chlamydia trachomatis , 1987, Infection and immunity.

[5]  R. W. Davis,et al.  Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. , 1998, Science.

[6]  C. Woese,et al.  Eubacterial origin of chlamydiae , 1986, Journal of bacteriology.

[7]  D. Raoult,et al.  Parachlamydiaceae: Potential Emerging Pathogens , 2002, Emerging infectious diseases.

[8]  T. Hatch,et al.  Characterization of late gene promoters of Chlamydia trachomatis , 1995, Journal of bacteriology.

[9]  D. Raoult,et al.  History of the ADP/ATP-Translocase-Encoding Gene, a Parasitism Gene Transferred from a Chlamydiales Ancestor to Plants 1 Billion Years Ago , 2004, Applied and Environmental Microbiology.

[10]  K. Everett,et al.  Molecular evolution of the Chlamydiaceae. , 2001, International journal of systematic and evolutionary microbiology.

[11]  S. Morgan,et al.  Muramic acid is not detectable in Chlamydia psittaci or Chlamydia trachomatis by gas chromatography-mass spectrometry , 1990, Infection and immunity.

[12]  H. Ochman,et al.  Bacterial genomes as new gene homes: the genealogy of ORFans in E. coli. , 2004, Genome research.

[13]  T. Hackstadt,et al.  Hc1‐mediated effects on DNA structure: a potential regulator of chlamydial development , 1993, Molecular microbiology.

[14]  K. Everett Chlamydia and Chlamydiales: more than meets the eye. , 2000, Veterinary microbiology.

[15]  N. Thomas,et al.  Plasmid diversity in Chlamydia. , 1997, Microbiology.

[16]  S. Giovannoni,et al.  The Order Planctomycetales and the Genera Planctomyces, Pirellula, Gemmata, and Isosphaera , 1992 .

[17]  T. Hatch Disulfide cross-linked envelope proteins: the functional equivalent of peptidoglycan in chlamydiae? , 1996, Journal of bacteriology.

[18]  T. Darville Chlamydia , 1998, Pediatrics In Review.

[19]  S. Salzberg,et al.  Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. , 2000, Nucleic acids research.

[20]  E. Bradbury,et al.  The chlamydial EUO gene encodes a histone H1-specific protease , 1997, Journal of bacteriology.

[21]  K. Everett,et al.  Architecture of the cell envelope of Chlamydia psittaci 6BC , 1995, Journal of bacteriology.

[22]  G. Perrière,et al.  The source of laterally transferred genes in bacterial genomes , 2003, Genome Biology.

[23]  M. Valassina,et al.  Increasing Diversity within Chlamydiae , 2003, Critical reviews in microbiology.

[24]  L. Koski,et al.  The Closest BLAST Hit Is Often Not the Nearest Neighbor , 2001, Journal of Molecular Evolution.

[25]  H. Hotzel,et al.  Detection of Chlamydia suis from clinical specimens: comparison of PCR, antigen ELISA, and culture. , 2003, Journal of microbiological methods.

[26]  Radhey S. Gupta,et al.  Signature proteins that are distinctive of alpha proteobacteria , 2005, BMC Genomics.

[27]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[28]  S. Salzberg,et al.  Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. , 2003, Nucleic acids research.

[29]  S. Birkelund,et al.  Genome and proteome analysis of Chlamydia , 2004, Proteomics.

[30]  M. Scidmore,et al.  Proteins in the chlamydial inclusion membrane. , 2002, Microbes and infection.

[31]  T. Hatch,et al.  Characterization of Outer Membrane Proteins in Chlamydia trachomatis LGV Serovar L2 , 2001, Journal of bacteriology.

[32]  Laura S. Frost,et al.  Mobile genetic elements: the agents of open source evolution , 2005, Nature Reviews Microbiology.

[33]  M. Starnbach,et al.  An Inclusion Membrane Protein from Chlamydia trachomatis Enters the MHC Class I Pathway and Stimulates a CD8+ T Cell Response 1 , 2003, The Journal of Immunology.

[34]  K. Schleifer,et al.  Phylogenetic Diversity among Geographically Dispersed Chlamydiales Endosymbionts Recovered from Clinical and Environmental Isolates of Acanthamoeba spp , 2000, Applied and Environmental Microbiology.

[35]  J. Ghuysen,et al.  Lack of Cell Wall Peptidoglycan versus Penicillin Sensitivity: New Insights into the Chlamydial Anomaly , 1999, Antimicrobial Agents and Chemotherapy.

[36]  W. Ludwig,et al.  Comparative phylogenetic analyses of members of the order Planctomycetales and the division Verrucomicrobia: 23S rRNA gene sequence analysis supports the 16S rRNA gene sequence-derived phylogeny. , 2000, International journal of systematic and evolutionary microbiology.

[37]  T. Hatch,et al.  Characterization of integration host factor (IHF) binding upstream of the cysteine‐rich protein operon (omcAB) promoter of Chlamydia trachomatis LGV serovar L2 , 2001, Molecular microbiology.

[38]  D. Kelly,et al.  The prokaryotes: an evolving electronic resource for the microbiological community - , 2002 .

[39]  D. Corsaro,et al.  Emerging Chlamydial Infections , 2004, Critical reviews in microbiology.

[40]  R. Stephens,et al.  Overexpression and surface localization of the Chlamydia trachomatis major outer membrane protein in Escherichia coli , 1992, Molecular microbiology.

[41]  T. McElwain,et al.  Analysis of the 16S rRNA gene of micro-organism 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. , 1999, International journal of systematic bacteriology.

[42]  Peer Bork,et al.  Functional clues for hypothetical proteins based on genomic context analysis in prokaryotes. , 2004, Nucleic acids research.

[43]  T. Hackstadt,et al.  Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early‐cycle development , 2003, Molecular microbiology.

[44]  M. Shimada,et al.  High Prevalence of Wolbachia in the Azuki Bean Beetle Callosobruchus chinensis (Coleoptera, Bruchidae) , 1999 .

[45]  T. Hatch,et al.  Characterization of a Chlamydia psittaciDNA Binding Protein (EUO) Synthesized during the Early and Middle Phases of the Developmental Cycle , 1998, Infection and Immunity.

[46]  N. Moran,et al.  Evolutionary Origins of Genomic Repertoires in Bacteria , 2005, PLoS biology.

[47]  J. Paavonen,et al.  The accuracy and efficacy of screening tests for Chlamydia trachomatis: a systematic review. , 2002, Journal of medical microbiology.

[48]  R. Stephens,et al.  Immune response to the Chlamydia trachomatis outer membrane protein PorB. , 2004, Vaccine.

[49]  B. Barrell,et al.  The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. , 2005, Genome research.

[50]  A. Andersen,et al.  Rapid Detection of the Chlamydiaceae and Other Families in the Order Chlamydiales: Three PCR Tests , 1999, Journal of Clinical Microbiology.

[51]  M. Wagner,et al.  Evidence for additional genus-level diversity of Chlamydiales in the environment. , 2001, FEMS microbiology letters.

[52]  R. Stephens,et al.  Genome Sequencing and Our Understanding of Chlamydiae , 2000, Infection and Immunity.

[53]  Radhey S. Gupta Protein Phylogenies and Signature Sequences: A Reappraisal of Evolutionary Relationships among Archaebacteria, Eubacteria, and Eukaryotes , 1998, Microbiology and Molecular Biology Reviews.

[54]  M. Horn,et al.  Neochlamydia hartmannellae gen. nov., sp. nov. (Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformis. , 2000, Microbiology.

[55]  M Bycroft,et al.  The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). , 2000, Journal of molecular biology.

[56]  Daniel Fischer,et al.  Twenty thousand ORFan microbial protein families for the biologist? , 2003, Structure.

[57]  Radhey S. Gupta,et al.  Protein signatures distinctive of chlamydial species: horizontal transfers of cell wall biosynthesis genes glmU from archaea to chlamydiae and murA between chlamydiae and Streptomyces. , 2002, Microbiology.

[58]  T. Hackstadt,et al.  Identification and characterization of a Chlamydia trachomatis early operon encoding four novel inclusion membrane proteins , 1999, Molecular microbiology.

[59]  D. Greenberg,et al.  High prevalence of "Simkania Z," a novel Chlamydia-like bacterium, in infants with acute bronchiolitis. , 1998, The Journal of infectious diseases.

[60]  D. Raoult,et al.  History of the ADP/ATP-Translocase-Encoding Gene, a Parasitism Gene Transferred from a Chlamydiales Ancestor to Plants 1 Billion Years Ago , 2003, Applied and Environmental Microbiology.

[61]  R. Gupta,et al.  The use of signature sequences in different proteins to determine the relative branching order of bacterial divisions: evidence that Fibrobacter diverged at a similar time to Chlamydia and the Cytophaga-Flavobacterium-Bacteroides division. , 2001, Microbiology.

[62]  Radhey S. Gupta,et al.  Protein Signatures Distinctive of Alpha Proteobacteria and Its Subgroups and a Model for α –Proteobacterial Evolution , 2005, Critical reviews in microbiology.

[63]  M. Comanducci,et al.  Diversity of the Chlamydia trachomatis common plasmid in biovars with different pathogenicity. , 1990, Plasmid.

[64]  Artem Cherkasov,et al.  Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. , 2002, Genome research.

[65]  Richard S. Stephens,et al.  Global Stage-Specific Gene Regulation during the Developmental Cycle of Chlamydia trachomatis , 2003, Journal of bacteriology.

[66]  M. Suyama,et al.  Evolution of prokaryotic gene order: genome rearrangements in closely related species. , 2001, Trends in genetics : TIG.

[67]  R. Heinzen,et al.  Origins and functions of the chlamydial inclusion. , 1997, Trends in microbiology.

[68]  Ronald W. Davis,et al.  Comparative genomes of Chlamydia pneumoniae and C. trachomatis , 1999, Nature Genetics.

[69]  P. Mårdh Chlamydia Screening‐Yes, but of Whom, When, by Whom, and with What? , 2000, Annals of the New York Academy of Sciences.

[70]  Radhey S. Gupta,et al.  Critical issues in bacterial phylogeny. , 2002, Theoretical population biology.

[71]  Radhey S. Gupta,et al.  Conserved indels in essential proteins that are distinctive characteristics of Chlamydiales and provide novel means for their identification. , 2005, Microbiology.

[72]  T. Hackstadt,et al.  Tandem genes of Chlamydia psittaci that encode proteins localized to the inclusion membrane , 1998, Molecular microbiology.

[73]  S. Henikoff,et al.  Amino acid substitution matrices from protein blocks. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[74]  B. Fane,et al.  Isolation, Molecular Characterisation and Genome Sequence of a Bacteriophage (Chp3) from Chlamydophila pecorum , 2004, Virus Genes.

[75]  T. Hatch Chlamydia: Old Ideas Crushed, New Mysteries Bared , 1998, Science.

[76]  A. Arakaki,et al.  Functional plasticity and catalytic efficiency in plant and bacterial ferredoxin-NADP(H) reductases. , 2004, Biochimica et biophysica acta.