Proteomics-based refinement of Deinococcus deserti genome annotation reveals an unwonted use of non-canonical translation initiation codons

Molecular and Cellular Proteomics

Volumn 9, Issue 2, 2010, Pages 415-426

  Baudet, Mathieu ^a   Ortet, Philippe ^b,c,d   Gaillard, Jean Charles ^a   Fernandez, Bernard ^a   Guérin, Philippe ^a   Enjalbal, Christine ^e   Subra, Gilles ^e   De Groot, Arjan ^b,c,d   Barakat, Mohamed ^b,c,d   Dedieu, Alain ^a   Armengaud, Jean ^a  

^a Institut de Biologie Environnementale et Biotechnologie   (France)

^b Institut de Biologie Environnementale et Biotechnologie   (France)

^c CNRS   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

^e UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

N TRIS(2,4,6 TRIMETHOXYPHENYL)PHOSPHONIUM ACETYLSUCCINIMIDE; PEPTIDE DERIVATIVE; REPLICATION INITIATOR PROTEIN DNAA; SUCCINIMIDE DERIVATIVE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENOME; CODON; CONTROLLED STUDY; DDRB GENE; DEIDE 03051 GENE; DEINOCOCCUS; DEINOCOCCUS DESERTI; DEINOCOCCUS GEOTHERMALIS; DEINOCOCCUS RADIODURANS; DNA REPAIR; GENOME ANALYSIS; INFC GENE; LIGA GENE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; POLA GENE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEOMICS; TRANSLATION INITIATION; VALIDATION PROCESS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CODON, INITIATOR; DATABASES, PROTEIN; DEINOCOCCUS; GENES, BACTERIAL; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; ORGANOPHOSPHORUS COMPOUNDS; PEPTIDES; PROTEIN BIOSYNTHESIS; PROTEIN SORTING SIGNALS; PROTEOMICS; SEQUENCE HOMOLOGY, AMINO ACID; STAINING AND LABELING;

BACTERIA (MICROORGANISMS); DEINOCOCCACEAE; DEINOCOCCUS DESERTI; DEINOCOCCUS GEOTHERMALIS; DEINOCOCCUS RADIODURANS; LIGA;

EID: 76649085822     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900359-MCP200     Document Type: Article

References (58)

1. Lima, T., Auchincloss, A. H., Coudert, E., Keller, G., Michoud, K., Rivoire, C., Bulliard, V., de Castro, E., Lachaize, C., Baratin, D., Phan, I., Bougueleret, L., and Bairoch, A. (2009) HAMAP: a database of completely sequenced microbial proteome sets and manually curated microbial protein families in UniProtKB/Swiss-Prot. Nucleic Acids Res. 37, D471-D478
2. Denoeud, F., Aury, J. M., Da Silva, C., Noel, B., Rogier, O., Delledonne, M., Morgante, M., Valle, G., Wincker, P., Scarpelli, C., Jaillon, O., and Artiguenave, F. (2008) Annotating genomes with massive-scale RNA sequencing. Genome Biol. 9, R175
3. Ansong, C., Purvine, S. O., Adkins, J. N., Lipton, M. S., and Smith, R. D. (2008) Proteogenomics: needs and roles to be filled by proteomics in genome annotation. Brief. Funct. Genomics Proteomics 7, 50-62
4. Armengaud, J. (2009) A perfect genome annotation is within reach with the proteomics and genomics alliance. Curr. Opin. Microbiol. 12, 292-300
5. Zivanovic, Y., Armengaud, J., Lagorce, A., Leplat, C., Guérin, P., Dutertre, M., Anthouard, V., Forterre, P., Wincker, P., and Confalonieri, F. (2009) Genome analysis and genome-wide proteomics of Thermococcus gammatolerans, the most radioresistant organism known amongst the Archaea. Genome Biol. 10, R70
6. Jaffe, J. D., Berg, H. C., and Church, G. M. (2004) Proteogenomic mapping as a complementary method to perform genome annotation. Proteomics 4, 59-77
7. Baerenfaller, K., Grossmann, J., Grobei, M. A., Hull, R., Hirsch-Hoffmann, M., Yalovsky, S., Zimmermann, P., Grossniklaus, U., Gruissem, W., and Baginsky, S. (2008) Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics. Science 320, 938-941
8. Bindschedler, L. V., Burgis, T. A., Mills, D. J., Ho, J. T., Cramer, R., and Spanu, P. D. (2009) In planta proteomics and proteogenomics of the biotrophic barley fungal pathogen blumeria graminis f. sp. hordei. Mol. Cell. Proteomics 8, 2368-2381
9. Castellana, N. E., Payne, S. H., Shen, Z., Stanke, M., Bafna, V., and Briggs, S. P. (2008) Discovery and revision of Arabidopsis genes by proteogenomics. Proc. Natl. Acad. Sci. U.S.A. 105, 21034-21038
10. Gupta, N., Benhamida, J., Bhargava, V., Goodman, D., Kain, E., Kerman, I., Nguyen, N., Ollikainen, N., Rodriguez, J., Wang, J., Lipton, M. S., Romine, M., Bafna, V., Smith, R. D., and Pevzner, P. A. (2008) Comparative proteogenomics: combining mass spectrometry and comparative genomics to analyze multiple genomes. Genome Res. 18, 1133-1142
11. Ishino, Y., Okada, H., Ikeuchi, M., and Taniguchi, H. (2007) Mass spectrometry-based prokaryote gene annotation. Proteomics 7, 4053-4065
12. Jungblut, P. R., Müller, E. C., Mattow, J., and Kaufmann, S. H. (2001) Proteomics reveals open reading frames in Mycobacterium tuberculosis H37Rv not predicted by genomics. Infect. Immun. 69, 5905-5907
13. Romine, M. F., Elias, D. A., Monroe, M. E., Auberry, K., Fang, R., Fredrickson, J. K., Anderson, G. A., Smith, R. D., and Lipton, M. S. (2004) Validation of Shewanella oneidensis MR-1 small proteins by AMT tagbased proteome analysis. Omics 8, 239-254
14. Shevchenko, A., Jensen, O. N., Podtelejnikov, A. V., Sagliocco, F., Wilm, M., Vorm, O., Mortensen, P., Shevchenko, A., Boucherie, H., and Mann, M. (1996) Linking genome and proteome by mass spectrometry: largescale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. U.S.A. 93, 14440-14445
15. Wright, J. C., Sugden, D., Francis-McIntyre, S., Riba-Garcia, I., Gaskell, S. J., Grigoriev, I. V., Baker, S. E., Beynon, R. J., and Hubbard, S. J. (2009) Exploiting proteomic data for genome annotation and gene model validation in Aspergillus niger. BMC Genomics 10, 61
16. Wang, R., Prince, J. T., and Marcotte, E. M. (2005) Mass spectrometry of the M. smegmatis proteome: protein expression levels correlate with function, operons, and codon bias. Genome Res. 15, 1118-1126
17. Deshayes, C., Perrodou, E., Gallien, S., Euphrasie, D., Schaeffer, C., Van-Dorsselaer, A., Poch, O., Lecompte, O., and Reyrat, J. M. (2007) Interrupted coding sequences in Mycobacterium smegmatis: authentic mutations or sequencing errors? Genome Biol. 8, R20
18. Gallien, S., Perrodou, E., Carapito, C., Deshayes, C., Reyrat, J. M., Van Dorsselaer, A., Poch, O., Schaeffer, C., and Lecompte, O. (2009) Orthoproteogenomics: multiple proteomes investigation through orthology and a new MS-based protocol. Genome Res. 19, 128-135
19. Yamazaki, S., Yamazaki, J., Nishijima, K., Otsuka, R., Mise, M., Ishikawa, H., Sasaki, K., Tago, S., and Isono, K. (2006) Proteome analysis of an aerobic hyperthermophilic crenarchaeon, Aeropyrum pernix K1. Mol. Cell. Proteomics 5, 811-823
20. Aivaliotis, M., Gevaert, K., Falb, M., Tebbe, A., Konstantinidis, K., Bisle, B., Klein, C., Martens, L., Staes, A., Timmerman, E., Van Damme, J., Siedler, F., Pfeiffer, F., Vandekerckhove, J., and Oesterhelt, D. (2007) Large-scale identification of N-terminal peptides in the halophilic archaea Halobacterium salinarum and Natronomonas pharaonis. J. Proteome Res. 6, 2195-2204
21. Gupta, N., Tanner, S., Jaitly, N., Adkins, J. N., Lipton, M., Edwards, R., Romine, M., Osterman, A., Bafna, V., Smith, R. D., and Pevzner, P. A. (2007) Whole proteome analysis of post-translational modifications: applications of mass-spectrometry for proteogenomic annotation. Genome Res. 17, 1362-1377
22. Gevaert, K., Goethals, M., Martens, L., Van Damme, J., Staes, A., Thomas, G. R., and Vandekerckhove, J. (2003) Exploring proteomes and analyzing protein processing by mass spectrometric identification of sorted Nterminal peptides. Nat. Biotechnol. 21, 566-569
23. Staes, A., Van Damme, P., Helsens, K., Demol, H., Vandekerckhove, J., and Gevaert, K. (2008) Improved recovery of proteome-informative, protein N-terminal peptides by combined fractional diagonal chromatography (COFRADIC). Proteomics 8, 1362-1370
24. Chen, W., Lee, P. J., Shion, H., Ellor, N., and Gebler, J. C. (2007) Improving de novo sequencing of peptides using a charged tag and C-terminal digestion. Anal. Chem. 79, 1583-1590
25. de Groot, A., Dulermo, R., Ortet, P., Blanchard, L., Guérin, P., Fernandez, B., Vacherie, B., Dossat, C., Jolivet, E., Siguier, P., Chandler, M., Barakat, M., Dedieu, A., Barbe, V., Heulin, T., Sommer, S., Achouak, W., and Armengaud, J. (2009) Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet. 5, e1000434
26. Cox, M. M., and Battista, J. R. (2005) Deinococcus radiodurans-the consummate survivor. Nat. Rev. Microbiol. 3, 882-892
27. Airo, A., Chan, S. L., Martinez, Z., Platt, M. O., and Trent, J. D. (2004) Heat shock and cold shock in Deinococcus radiodurans. Cell. Biochem. Biophys. 40, 277-288
28. Lipton, M. S., Pasa-Tolic', L., Anderson, G. A., Anderson, D. J., Auberry, D. L., Battista, J. R., Daly, M. J., Fredrickson, J., Hixson, K. K., Kostandarithes, H., Masselon, C., Markillie, L. M., Moore, R. J., Romine, M. F., Shen, Y., Stritmatter, E., Tolic', N., Udseth, H. R., Venkateswaran, A., Wong, K. K., Zhao, R., and Smith, R. D. (2002) Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc. Natl. Acad. Sci. U.S.A. 99, 11049-11054
29. Lipton, M. S., Romine, M. F., Monroe, M. E., Elias, D. A., Pasa-Tolic, L., Anderson, G. A., Anderson, D. J., Fredrickson, J., Hixson, K. K., Masselon, C., Mottaz, H., Tolic, N., and Smith, R. D. (2006) AMT tag approach to proteomic characterization of Deinococcus radiodurans and Shewanella oneidensis. Methods Biochem. Anal. 49, 113-134
30. Lu, H., Gao, G., Xu, G., Fan, L., Yin, L., Shen, B., and Hua, Y. (2009) Deinococcus radiodurans PprI switches on DNA damage response and cellular survival networks after radiation damage. Mol. Cell. Proteomics 8, 481-494
31. Schmid, A. K., Lipton, M. S., Mottaz, H., Monroe, M. E., Smith, R. D., and Lidstrom, M. E. (2005) Global whole-cell FTICR mass spectrometric proteomics analysis of the heat shock response in the radioresistant bacterium Deinococcus radiodurans. J. Proteome Res. 4, 709-718
32. Zhang, C., Wei, J., Zheng, Z., Ying, N., Sheng, D., and Hua, Y. (2005) Proteomic analysis of Deinococcus radiodurans recovering from gamma-irradiation. Proteomics 5, 138-143
33. White, O., Eisen, J. A., Heidelberg, J. F., Hickey, E. K., Peterson, J. D., Dodson, R. J., Haft, D. H., Gwinn, M. L., Nelson, W. C., Richardson, D. L., Moffat, K. S., Qin, H., Jiang, L., Pamphile, W., Crosby, M., Shen, M., Vamathevan, J. J., Lam, P., McDonald, L., Utterback, T., Zalewski, C., Makarova, K. S., Aravind, L., Daly, M. J., Minton, K. W., Fleischmann, R. D., Ketchum, K. A., Nelson, K. E., Salzberg, S., Smith, H. O., Venter, J. C., and Fraser, C. M. (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286, 1571-1577
34. Makarova, K. S., Omelchenko, M. V., Gaidamakova, E. K., Matrosova, V. Y., Vasilenko, A., Zhai, M., Lapidus, A., Copeland, A., Kim, E., Land, M., Mavrommatis, K., Pitluck, S., Richardson, P. M., Detter, C., Brettin, T., Saunders, E., Lai, B., Ravel, B., Kemner, K. M., Wolf, Y. I., Sorokin, A., Gerasimova, A. V., Gelfand, M. S., Fredrickson, J. K., Koonin, E. V., and Daly, M. J. (2007) Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS ONE 2, e955
35. Henne, A., Brüggemann, H., Raasch, C., Wiezer, A., Hartsch, T., Liesegang, H., Johann, A., Lienard, T., Gohl, O., Martinez-Arias, R., Jacobi, C., Starkuviene, V., Schlenczeck, S., Dencker, S., Huber, R., Klenk, H. P., Kramer, W., Merkl, R., Gottschalk, G., and Fritz, H. J. (2004) The genome sequence of the extreme thermophile Thermus thermophilus. Nat. Biotechnol. 22, 547-553
36. Dupierris, V., Masselon, C., Court, M., Kieffer-Jaquinod, S., and Bruley, C. (2009) A toolbox for validation of mass spectrometry peptides identification and generation of database: IRMa. Bioinformatics 25, 1980-1981
37. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2, 953-971
38. Juncker, A. S., Willenbrock, H., Von Heijne, G., Brunak, S., Nielsen, H., and Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 12, 1652-1662
39. Rose, R. W., Brüser, T., Kissinger, J. C., and Pohlschröder, M. (2002) Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol. Microbiol. 45, 943-950
40. Jones, P., Cǒ té, R. G., Cho, S. Y., Klie, S., Martens, L., Quinn, A. F., Thorneycroft, D., and Hermjakob, H. (2008) PRIDE: new developments and new datasets. Nucleic Acids Res. 36, D878-D883
41. Nguyen, H. H., de la Tour, C. B., Toueille, M., Vannier, F., Sommer, S., and Servant, P. (2009) The essential histone-like protein HU plays a major role in Deinococcus radiodurans nucleoid compaction. Mol. Microbiol. 73, 240-252
42. Binns, N., and Masters, M. (2002) Expression of the Escherichia coli pcnB gene is translationally limited using an inefficient start codon: a second chromosomal example of translation initiated at AUU. Mol. Microbiol. 44, 1287-1298
43. Hatfield, D., and Diamond, A. (1993) UGA: a split personality in the universal genetic code. Trends Genet. 9, 69-70
44. Liveris, D., Schwartz, J. J., Geertman, R., and Schwartz, I. (1993) Molecular cloning and sequencing of infC, the gene encoding translation initiation factor IF3, from four enterobacterial species. FEMS Microbiol. Lett. 112, 211-216
45. Polard, P., Prère, M. F., Chandler, M., and Fayet, O. (1991) Programmed translational frameshifting and initiation at an AUU codon in gene expression of bacterial insertion sequence IS911. J. Mol. Biol. 222, 465-477
46. Sazuka, T., and Ohara, O. (1996) Sequence features surrounding the translation initiation sites assigned on the genome sequence of Synechocystis sp. strain PCC6803 by amino-terminal protein sequencing. DNA Res. 3, 225-232
47. Spiers, A. J., and Bergquist, P. L. (1992) Expression and regulation of the RepA protein of the RepFIB replicon from plasmid P307. J. Bacteriol. 174, 7533-7541
48. Butler, J. S., Springer, M., and Grunberg-Manago, M. (1987) AUU-to-AUG mutation in the initiator codon of the translation initiation factor IF3 abolishes translational autocontrol of its own gene (infC) in vivo. Proc. Natl. Acad. Sci. U.S.A. 84, 4022-4025
49. Blaszczyk, J., Li, Y., Cherry, S., Alexandratos, J., Wu, Y., Shaw, G., Tropea, J. E., Waugh, D. S., Yan, H., and Ji, X. (2007) Structure and activity of Yersinia pestis 6-hydroxymethyl-7,8-dihydropterin pyrophosphokinase as a novel target for the development of antiplague therapeutics. Acta Crystallogr. Sect. D Biol. Crystallogr. 63, 1169-1177
50. Restrepo-Montoya, D., Vizcaíno, C., Niño, L. F., Ocampo, M., Patarroyo, M. E., and Patarroyo, M. A. (2009) Validating subcellular localization prediction tools with mycobacterial proteins. BMC Bioinformatics 10, 134
51. Battista, J. R., Park, M. J., and McLemore, A. E. (2001) Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology 43, 133-139
52. Blasius, M., Sommer, S., and Hübscher, U. (2008) Deinococcus radiodurans: what belongs to the survival kit? Crit. Rev. Biochem. Mol. Biol. 43, 221-238
53. Daly, M. J. (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat. Rev. Microbiol. 7, 237-245
54. Daly, M. J., Gaidamakova, E. K., Matrosova, V. Y., Vasilenko, A., Zhai, M., Venkateswaran, A., Hess, M., Omelchenko, M. V., Kostandarithes, H. M., Makarova, K. S., Wackett, L. P., Fredrickson, J. K., and Ghosal, D. (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates gammaradiation resistance. Science 306, 1025-1028
55. Zahradka, K., Slade, D., Bailone, A., Sommer, S., Averbeck, D., Petranovic, M., Lindner, A. B., and Radman, M. (2006) Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443, 569-573
56. Norais, C. A., Chitteni-Pattu, S., Wood, E. A., Inman, R. B., and Cox, M. M. (2009) An alternative Deinococcus radiodurans SSB induced by ionizing radiation: the DdrB protein. J. Biol. Chem. 284, 21402-21411
57. Berthon, J., Cortez, D., and Forterre, P. (2008) Genomic context analysis in Archaea suggests previously unrecognized links between DNA replication and translation. Genome Biol. 9, R71
58. Berthon, J., Fujikane, R., and Forterre, P. (2009) When DNA replication and protein synthesis come together. Trends Biochem. Sci. 34, 429-434