Proteomic analysis reveals a virtually complete set of proteins for translation and energy generation in elementary bodies of the amoeba symbiont Protochlamydia amoebophila

Proteomics

Volumn 11, Issue 10, 2011, Pages 1868-1892

  Sixt, Barbara S ^a   Heinz, Christian ^a   Pichler, Peter ^a   Heinz, Eva ^a   Montanaro, Jacqueline ^a   Op den Camp, Huub J M ^b   Ammerer, Gustav ^a   Mechtler, Karl ^c   Wagner, Michael ^a   Horn, Matthias ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

Author keywords

2 DE; Amoeba; Chlamydia; Microbiology; Shotgun proteomics; Symbiont

Indexed keywords

PROTEOME;

ACANTHAMOEBA; AMOEBA (GENUS); ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; CHLAMYDIA; COMPARATIVE STUDY; ENERGY; GENE SEQUENCE; GENETIC TRANSCRIPTION; HOST PATHOGEN INTERACTION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; PROTOCHLAMYDIA AMOEBOPHILA; RNA TRANSLATION; SYMBIONT;

ACANTHAMOEBA; BACTERIAL PROTEINS; CHLAMYDIALES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENERGY METABOLISM; METABOLIC NETWORKS AND PATHWAYS; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDE MAPPING; PROTEIN BIOSYNTHESIS; PROTEOME; PROTEOMICS; SYMBIOSIS; TRANSCRIPTION, GENETIC;

ACANTHAMOEBA; ANIMALIA; BACTERIA (MICROORGANISMS); CANDIDATUS PROTOCHLAMYDIA AMOEBOPHILA; CHLAMYDIA; CHLAMYDIACEAE; CHLAMYDIAE; PARACHLAMYDIACEAE; PROTOZOA; VERTEBRATA;

EID: 79955753888     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000510     Document Type: Article

References (69)

1. Bebear, C., de Barbeyrac, B., Genital Chlamydia trachomatis infections. Clin. Microbiol. Infect. 2009, 15, 4-10.
2. Wright, H. R., Turner, A., Taylor, H. R., Trachoma. Lancet 2008, 371, 1945-1954.
3. Blasi, F., Tarsia, P., Aliberti, S., Chlamydophila pneumoniae. Clin. Microbiol. Infect. 2009, 15, 29-35.
4. Amann, R., Springer, N., Schonhuber, W., Ludwig, W. et al., Obligate intracellular bacterial parasites of acanthamoebae related to Chlamydia spp. Appl. Environ. Microbiol. 1997, 63, 115-121.
5. Horn, M., Chlamydiae as symbionts in eukaryotes. Annu. Rev. Microbiol. 2008, 62, 113-131.
6. Abdelrahman, Y. M., Belland, R. J., The chlamydial developmental cycle. FEMS Microbiol. Rev. 2005, 29, 949-959.
7. Corsaro, D., Greub, G., Pathogenic potential of novel Chlamydiae and diagnostic approaches to infections due to these obligate intracellular bacteria. Clin. Microbiol. Rev. 2006, 19, 283-297.
8. Greub, G., Parachlamydia acanthamoebae, an emerging agent of pneumonia. Clin. Microbiol. Infect. 2009, 15, 18-28.
9. Haider, S., Collingro, A., Walochnik, J., Wagner, M., Horn, M., Chlamydia-like bacteria in respiratory samples of community-acquired pneumonia patients. FEMS Microbiol. Lett. 2008, 281, 198-202.
10. Horn, M., Collingro, A., Schmitz-Esser, S., Beier, C. L. et al., Illuminating the evolutionary history of chlamydiae. Science 2004, 304, 728-730.
11. Heinz, E., Tischler, P., Rattei, T., Myers, G. et al., Comprehensive in silico prediction and analysis of chlamydial outer membrane proteins reflects evolution and life style of the Chlamydiae. Biomed. Chromatogr. Genomics 2009, 10, 634.
12. Heinz, E., Pichler, P., Heinz, C., op den Camp, H. J. M. et al., Proteomic analysis of the outer membrane of Protochlamydia amoebophila elementary bodies. Proteomics 2010, 10, 4363-4376.
13. Heuer, D., Kneip, C., Maurer, A. P., Meyer, T. F., Tackling the intractable - approaching the genetics of Chlamydiales. Int. J. Med. Microbiol. 2007, 297, 569-576.
14. Greub, G., Kebbi-Beghdadi, C., Bertelli, C., Collyn, F. et al., High throughput sequencing and proteomics to identify immunogenic proteins of a new pathogen: the dirty genome approach. PLoS One 2009, 4, e8423.
15. Liu, X., Afrane, M., Clemmer, D. E., Zhong, G., Nelson, D. E., Identification of Chlamydia trachomatis outer membrane complex proteins by differential proteomics. J. Bacteriol. 2010, 192, 2852-2860.
16. Shaw, A. C., Gevaert, K., Demol, H., Hoorelbeke, B. et al., Comparative proteome analysis of Chlamydia trachomatis serovar A, D and L2. Proteomics 2002, 2, 164-186.
17. Skipp, P., Robinson, J., O'Connor, C. D., Clarke, I. N., Shotgun proteomic analysis of Chlamydia trachomatis. Proteomics 2005, 5, 1558-1573.
18. Vandahl, B. B., Birkelund, S., Demol, H., Hoorelbeke, B. et al., Proteome analysis of the Chlamydia pneumoniae elementary body. Electrophoresis 2001, 22, 1204-1223.
19. Jungblut, P. R., Holzhütter, H. G., Apweiler, R., Schlüter, H., The speciation of the proteome. Chem. Cent. J. 2008, 2, 16.
20. Schlüter, H., Apweiler, R., Holzhütter, H. G., Jungblut, P. R., Finding one's way in proteomics: a protein species nomenclature. Chem. Cent. J. 2009, 3, 11.
21. Kelleher, N. L., Lin, H. Y., Valaskovic, G. A., Aaserud, D. J. et al., Top down versus bottom up protein characterization by tandem high-resolution mass spectrometry. J. Am. Chem. Soc. 1999, 121, 806-812.
22. Nesvizhskii, A. I., Protein identification by tandem mass spectrometry and sequence database searching. Methods Mol. Biol. 2007, 367, 87-119.
23. Haider, S., Wagner, M., Schmid, M. C., Sixt, B. S. et al., Raman microspectroscopy reveals long-term extracellular activity of chlamydiae. Mol. Microbiol. 2010, 77, 687-700.
24. Collingro, A., Toenshoff, E. R., Taylor, M. W., Fritsche, T. R. et al., "Candidatus Protochlamydia amoebophila", an endosymbiont of Acanthamoeba spp. Int. J. Syst. Evol. Microbiol. 2005, 55, 1863-1866.
25. Vandahl, B. B., Birkelund, S., Christiansen, G., Proteome analysis of Chlamydia pneumoniae. Methods Enzymol. 2002, 358, 277-288.
26. Herbert, B. R., Grinyer, J., McCarthy, J. T., Isaacs, M. et al., Improved 2-DE of microorganisms after acidic extraction. Electrophoresis 2006, 27, 1630-1640.
27. Neuhoff, V., Stamm, R., Eibl, H., Clear background and highly sensitive protein staining with Coomassie Blue dyes in polyacrylamide gels - a systematic analysis. Electrophoresis 1985, 6, 427-448.
28. Blum, H., Beier, H., Gross, H. J., Improved silver staining of plant-proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 1987, 8, 93-99.
29. Anderson, I. J., Watkins, R. F., Samuelson, J., Spencer, D. F. et al., Gene discovery in the Acanthamoeba castellanii genome. Protist 2005, 156, 203-214.
30. Loftus, B., Anderson, I., Davies, R., Alsmark, U. C. et al., The genome of the protist parasite Entamoeba histolytica. Nature 2005, 433, 865-868.
31. Eichinger, L., Pachebat, J. A., Glockner, G., Rajandream, M. A. et al., The genome of the social amoeba Dictyostelium discoideum. Nature 2005, 435, 43-57.
32. Vizcaino, J. A., Cote, R., Reisinger, F., Foster, J. M. et al., A guide to the Proteomics Identifications Database proteomics data repository. Proteomics 2009, 9, 4276-4283.
33. Barsnes, H., Vizcaino, J. A., Eidhammer, I., Martens, L., PRIDE Converter: making proteomics data-sharing easy. Nat. Biotechnol. 2009, 27, 598-599.
34. Hoogland, C., Mostaguir, K., Appel, R. D., Lisacek, F., The World-2DPAGE Constellation to promote and publish gel-based proteomics data through the ExPASy server. J. Proteomics 2008, 71, 245-248.
35. Miller, I., Crawford, J., Gianazza, E., Protein stains for proteomic applications: which, when, why? Proteomics 2006, 6, 5385-5408.
36. Görg, A., Weiss, W., Dunn, M. J., Current two-dimensional electrophoresis technology for proteomics. Proteomics 2004, 4, 3665-3685.
37. Berven, F. S., Karlsen, O. A., Murrell, J. C., Jensen, H. B., Multiple polypeptide forms observed in two-dimensional gels of Methylococcus capsulatus (Bath) polypeptides are generated during the separation procedure. Electrophoresis 2003, 24, 757-761.
38. Birkelund, S., Vandahl, B., Christiansen, G., in: Bavoil, P. M., Wyrick, P. B. (Eds.), Chlamydia: Genomics and Pathogenesis, Horizon Bioscience, Norfolk, UK 2006, pp. 45-58.
39. Righetti, P. G., Real and imaginary artefacts in proteome analysis via two-dimensional maps. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2006, 841, 14-22.
40. Görg, A., Drews, O., Luck, C., Weiland, F., Weiss, W., 2-DE with IPGs. Electrophoresis 2009, 30, S122-S132.
41. Vercauteren, F. G., Arckens, L., Quirion, R., Applications and current challenges of proteomic approaches, focusing on two-dimensional electrophoresis. Amino Acids 2007, 33, 405-414.
42. Wolters, D. A., Washburn, M. P., Yates, J. R., 3rd, An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 2001, 73, 5683-5690.
43. Helbig, A. O., Heck, A. J., Slijper, M., Exploring the membrane proteome - challenges and analytical strategies. J. Proteomics 2010, 73, 868-878.
44. Lu, B., McClatchy, D. B., Kim, J. Y., Yates, J. R., 3rd, Strategies for shotgun identification of integral membrane proteins by tandem mass spectrometry. Proteomics 2008, 8, 3947-3955.
45. Riley, M. L., Schmidt, T., Artamonova, I. I., Wagner, C. et al., PEDANT genome database: 10 years online. Nucleic Acids Res. 2007, 35, D354-D357.
46. Jungblut, P. R., Schiele, F., Zimny-Arndt, U., Ackermann, R. et al., Helicobacter pylori proteomics by 2-DE/MS, 1-DE-LC/MS and functional data mining. Proteomics 2010, 10, 182-193.
47. Rabilloud, T., Chevallet, M., Luche, S., Lelong, C., Fully denaturing two-dimensional electrophoresis of membrane proteins: a critical update. Proteomics 2008, 8, 3965-3973.
48. Barry, C. E., Hayes, S. F., Hackstadt, T., Nucleoid condensation in Escherichia coli that express a chlamydial histone homolog. Science 1992, 256, 377-379.
49. Vandahl, B. B., Birkelund, S., Christiansen, G., Genome and proteome analysis of Chlamydia. Proteomics 2004, 4, 2831-2842.
50. Matsumoto, A., in: Barron, A. L. (Ed.), Microbiology of Chlamydia, CRC Press, Inc., Boca Raton, FL 1988, pp. 21-45.
51. Tamura, A., Matsumoto, A., Manire, G. P., Higashi, N., Electron microscopic observations on the structure of the envelopes of mature elementary bodies and developmental reticulate forms of Chlamydia psittaci. J. Bacteriol. 1971, 105, 355-360.
52. McClarty, G., in: Stephens, R. S. (Ed.), Chlamydia, American Society for Microbiology, Washington DC 1999, pp. 69-100.
53. Schmitz-Esser, S., Linka, N., Collingro, A., Beier, C. L. et al., ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J. Bacteriol. 2004, 186, 683-691.
54. Haferkamp, I., Schmitz-Esser, S., Wagner, M., Neigel, N. et al., Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol. Microbiol. 2006, 60, 1534-1545.
55. + transporter in an intracellular bacterial symbiont related to Chlamydiae. Nature 2004, 432, 622-625.
56. Ghuysen, J. M., Goffin, C., Lack of cell wall peptidoglycan versus penicillin sensitivity: new insights into the chlamydial anomaly. Antimicrob. Agents Chemother. 1999, 43, 2339-2344.
57. Chopra, I., Storey, C., Falla, T. J., Pearce, J. H., Antibiotics, peptidoglycan synthesis and genomics: the chlamydial anomaly revisited. Microbiology 1998, 144, 2673-2678.
58. Horn, M., Collingro, A., Schmitz-Esser, S., Wagner, M., in: Bavoil, P. M., Wyrick, P. B. (Eds.), Chlamydia: Genomics and Pathogenesis, Horizon Bioscience, Norfolk, UK 2006, pp. 25-44.
59. Hatch, T. P., in: Stephens, R. S. (Ed.), Chlamydia, American Society for Microbiology, Washington, DC 1999, pp. 29-67.
60. Peters, J., Wilson, D. P., Myers, G., Timms, P., Bavoil, P. M., Type III secretion à la Chlamydia. Trends Microbiol. 2007, 15, 241-251.
61. Fields, K. A., Mead, D. J., Dooley, C. A., Hackstadt, T., Chlamydia trachomatis type III secretion: evidence for a functional apparatus during early-cycle development. Mol. Microbiol. 2003, 48, 671-683.
62. Greub, G., Collyn, F., Guy, L., Roten, C. A., A genomic island present along the bacterial chromosome of the Parachlamydiaceae UWE25, an obligate amoebal endosymbiont, encodes a potentially functional F-like conjugative DNA transfer system. Biomed. Chromatogr. Microbiol. 2004, 4, 48.
63. Heinz, E., Rockey, D. D., Montanaro, J., Aistleitner, K. et al., Inclusion membrane proteins of Protochlamydia amoebophila UWE25 reveal a conserved mechanism for host cell interaction among the Chlamydiae. J. Bacteriol. 2010, 192, 5093-5102.
64. Brinkman, F. S., Blanchard, J. L., Cherkasov, A., Av-Gay, Y. et al., Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Res. 2002, 12, 1159-1167.
65. Huang, J., Gogarten, J., Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? Genome Biol. 2007, 8, R99.
66. Moustafa, A., Reyes-Prieto, A., Bhattacharya, A., Chlamydiae has contributed at least 55 genes to Plantae with predominantly plastid functions. PloS ONE 2008, 3, e2205.
67. Tyra, H. M., Linka, M., Weber, A. P., Bhattacharya, D., Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol. 2007, 8, R212.
68. Bordenstein, S. R., Reznikoff, W. S., Mobile DNA in obligate intracellular bacteria. Nat. Rev. Microbiol. 2005, 3, 688-699.
69. Lehnherr, H., Maguin, E., Jafri, S., Yarmolinsky, M. B., Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J. Mol. Biol. 1993, 233, 414-428.