Home LiteratureArticle Details
PMID: 17690205 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Whole proteome analysis of post-translational modifications: applications of mass-spectrometry for proteogenomic annotation.

Genome research ·Vol. 17 ·No. 9 ·2007-09-00 ·Pages 1362-77

Gupta N, Tanner S, Jaitly N, Adkins JN, Lipton M, Edwards R, Romine M, Osterman A, Bafna V, Smith RD, Pevzner PA

Abstract

While bacterial genome annotations have significantly improved in recent years, techniques for bacterial proteome annotation (including post-translational chemical modifications, signal peptides, proteolytic events, etc.) are still in their infancy. At the same time, the number of sequenced bacterial genomes is rising sharply, far outpacing our ability to validate the predicted genes, let alone annotate bacterial proteomes. In this study, we use tandem mass spectrometry (MS/MS) to annotate the proteome of Shewanella oneidensis MR-1, an important microbe for bioremediation. In particular, we provide the first comprehensive map of post-translational modifications in a bacterial genome, including a large number of chemical modifications, signal peptide cleavages, and cleavages of N-terminal methionine residues. We also detect multiple genes that were missed or assigned incorrect start positions by gene prediction programs, and suggest corrections to improve the gene annotation. This study demonstrates that complementing every genome sequencing project by an MS/MS project would significantly improve both genome and proteome annotations for a reasonable cost.

MeSH Terms
Amino Acid Sequence Cytoskeletal Proteins/chemistry Eye Proteins/chemistry Genome, Bacterial Genomics/methods Glycoproteins/chemistry Mass Spectrometry/methods Models, Biological Molecular Sequence Data Peptides/chemistry Protein Processing, Post-Translational Proteome/analysis Proteomics/methods Sequence Homology, Amino Acid Shewanella/genetics Tandem Mass Spectrometry
Chemicals
Cytoskeletal Proteins Eye Proteins Glycoproteins Peptides Proteome trabecular meshwork-induced glucocorticoid response protein
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Gupta Nitin
Bioinformatics Program, University of California San Diego, La Jolla, California 92093, USA. nguta@ucsd.edu
Tanner Stephen
Jaitly Navdeep
Adkins Joshua N
Lipton Mary
Edwards Robert
Romine Margaret
Osterman Andrei
Bafna Vineet
Smith Richard D
Pevzner Pavel A
References (87)
87 references, click to expand
  1. Experimental determination and system level analysis of essential genes in Escherichia coli MG1655.
    J Bacteriol. 2003 Oct;185(19):5673-84 PMID: 13129938
  2. Reannotation of Shewanella oneidensis genome.
    OMICS. 2003 Summer;7(2):171-5 PMID: 14506846
  3. Proteogenomic mapping as a complementary method to perform genome annotation.
    Proteomics. 2004 Jan;4(1):59-77 PMID: 14730672
  4. Comparative genomics, minimal gene-sets and the last universal common ancestor.
    Nat Rev Microbiol. 2003 Nov;1(2):127-36 PMID: 15035042
  5. Environmental genome shotgun sequencing of the Sargasso Sea.
    Science. 2004 Apr 2;304(5667):66-74 PMID: 15001713
  6. Methylation of ribosomal proteins during ribosome assembly in Escherichia coli.
    Mol Gen Genet. 1981;183(3):418-21 PMID: 7038376
  7. Multiple covalent modifications of Trg, a sensory transducer of Escherichia coli.
    J Biol Chem. 1983 Apr 25;258(8):5050-5 PMID: 6300110
  8. Sequence of a 1.26-kb DNA fragment containing the structural gene for E.coli initiation factor IF3: presence of an AUU initiator codon.
    EMBO J. 1982;1(3):311-5 PMID: 6325158
  9. Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure.
    J Bacteriol. 1987 Feb;169(2):751-7 PMID: 3027045
  10. Cloning and characterization of a gene cluster from Bacillus stearothermophilus comprising infC, rpmI and rplT.
    Mol Gen Genet. 1989 Aug;218(2):355-7 PMID: 2779520
  11. Influence of ions on cyclization of the amino terminal glutamine residues of tryptic peptides of streptococcal PepM49 protein. Resolution of cyclized peptides by HPLC and characterization by mass spectrometry.
    Int J Pept Protein Res. 1989 Aug;34(2):118-23 PMID: 2807728
  12. Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid.
    Proc Natl Acad Sci U S A. 1989 Nov;86(21):8247-51 PMID: 2682640
  13. Strategies for determination of disulphide bridges in proteins using plasma desorption mass spectrometry.
    Biomed Environ Mass Spectrom. 1990 Nov;19(11):713-20 PMID: 2076469
  14. Sites of deamidation and methylation in Tsr, a bacterial chemotaxis sensory transducer.
    J Biol Chem. 1991 May 25;266(15):9746-53 PMID: 2033064
  15. Genome annotation of Anopheles gambiae using mass spectrometry-derived data.
    BMC Genomics. 2005;6:128 PMID: 16171517
  16. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes.
    Nucleic Acids Res. 2005;33(17):5691-702 PMID: 16214803
  17. Identification of an artifact in the mass spectrometry of proteins derivatized with iodoacetamide.
    J Mass Spectrom. 2000 Apr;35(4):572-5 PMID: 10797654
  18. Deamidation as a widespread phenomenon in two-dimensional polyacrylamide gel electrophoresis of human blood plasma proteins.
    Electrophoresis. 2000 Jun;21(11):2209-18 PMID: 10892731
  19. The Comprehensive Microbial Resource.
    Nucleic Acids Res. 2001 Jan 1;29(1):123-5 PMID: 11125067
  20. Use of mass spectrometry-derived data to annotate nucleotide and protein sequence databases.
    Trends Biochem Sci. 2001 Jan;26(1):54-61 PMID: 11165518
  21. Overalkylation of a protein digest with iodoacetamide.
    Anal Chem. 2001 Aug 1;73(15):3576-82 PMID: 11510821
  22. A proteomic view on genome-based signal peptide predictions.
    Genome Res. 2001 Sep;11(9):1484-502 PMID: 11544192
  23. Mass spectrometry allows direct identification of proteins in large genomes.
    Proteomics. 2001 May;1(5):641-50 PMID: 11678034
  24. WebLogo: a sequence logo generator.
    Genome Res. 2004 Jun;14(6):1188-90 PMID: 15173120
  25. The RESID Database of Protein Modifications as a resource and annotation tool.
    Proteomics. 2004 Jun;4(6):1527-33 PMID: 15174122
  26. Unimod: Protein modifications for mass spectrometry.
    Proteomics. 2004 Jun;4(6):1534-6 PMID: 15174123
  27. Trypsin cleaves exclusively C-terminal to arginine and lysine residues.
    Mol Cell Proteomics. 2004 Jun;3(6):608-14 PMID: 15034119
  28. PrediSi: prediction of signal peptides and their cleavage positions.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W375-9 PMID: 15215414
  29. Improved prediction of signal peptides: SignalP 3.0.
    J Mol Biol. 2004 Jul 16;340(4):783-95 PMID: 15223320
  30. The complete genome and proteome of Mycoplasma mobile.
    Genome Res. 2004 Aug;14(8):1447-61 PMID: 15289470
  31. Methylation of the flagellin of Salmonella typhimurium.
    J Bacteriol. 1971 Jan;105(1):211-9 PMID: 5541007
  32. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites.
    Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342-6 PMID: 4598299
  33. Dipeptidyl carboxypeptidase from Escherichia coli.
    Methods Enzymol. 1976;45:599-610 PMID: 13271
  34. Isolation of glutamic acid methyl ester from an Escherichia coli membrane protein involved in chemotaxis.
    J Biol Chem. 1977 May 25;252(10):3214-8 PMID: 16888
  35. Location of the site of methylation in elongation factor Tu.
    FEBS Lett. 1979 Nov 15;107(2):359-62 PMID: 389663
  36. Purified human growth hormone from E. coli is biologically active.
    Nature. 1981 Oct 1;293(5831):408-11 PMID: 7024824
  37. Amino acids responsible for flagellar shape are distributed in terminal regions of flagellin.
    J Mol Biol. 1991 Jun 5;219(3):471-80 PMID: 2051483
  38. Translation of the flagellar gene fliO of Salmonella typhimurium from putative tandem starts.
    J Bacteriol. 1998 Jun;180(11):2936-42 PMID: 9603885
  39. The identification of peptide modifications derived from gel-separated proteins using electrospray triple quadrupole and ion trap analyses.
    Electrophoresis. 1998 May;19(6):989-97 PMID: 9638945
  40. Small genes/gene-products in Escherichia coli K-12.
    FEMS Microbiol Lett. 1998 Dec 15;169(2):375-82 PMID: 9868784
  41. Carbamylation of cysteine: a potential artifact in peptide mapping of hemoglobins in the presence of urea.
    Anal Biochem. 1999 Feb 1;267(1):57-64 PMID: 9918655
  42. Observation of Escherichia coli ribosomal proteins and their posttranslational modifications by mass spectrometry.
    Anal Biochem. 1999 Apr 10;269(1):105-12 PMID: 10094780
  43. High-throughput mass spectrometric discovery of protein post-translational modifications.
    J Mol Biol. 1999 Jun 11;289(3):645-57 PMID: 10356335
  44. Validation of Shewanella oneidensis MR-1 small proteins by AMT tag-based proteome analysis.
    OMICS. 2004 Fall;8(3):239-54 PMID: 15669716
  45. Global profiling of Shewanella oneidensis MR-1: expression of hypothetical genes and improved functional annotations.
    Proc Natl Acad Sci U S A. 2005 Feb 8;102(6):2099-104 PMID: 15684069
  46. Identification of degradation products formed during performic oxidation of peptides and proteins by high-performance liquid chromatography with matrix-assisted laser desorption/ionization and tandem mass spectrometry.
    Rapid Commun Mass Spectrom. 2005;19(9):1130-8 PMID: 15799070
  47. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses.
    Nucleic Acids Res. 2005 Jul 1;33(Web Server issue):W451-4 PMID: 15980510
  48. InsPecT: identification of posttranslationally modified peptides from tandem mass spectra.
    Anal Chem. 2005 Jul 15;77(14):4626-39 PMID: 16013882
  49. Mass spectrometry of the M. smegmatis proteome: protein expression levels correlate with function, operons, and codon bias.
    Genome Res. 2005 Aug;15(8):1118-26 PMID: 16077011
  50. Global detection and characterization of hypothetical proteins in Shewanella oneidensis MR-1 using LC-MS based proteomics.
    Proteomics. 2005 Aug;5(12):3120-30 PMID: 16038018
  51. Characterization of intact microorganisms by MALDI mass spectrometry.
    Mass Spectrom Rev. 2001 Jul-Aug;20(4):157-71 PMID: 11835304
  52. The hemK gene in Escherichia coli encodes the N(5)-glutamine methyltransferase that modifies peptide release factors.
    EMBO J. 2002 Feb 15;21(4):769-78 PMID: 11847124
  53. Recoding: translational bifurcations in gene expression.
    Gene. 2002 Mar 20;286(2):187-201 PMID: 11943474
  54. The N-end rule in bacteria.
    Science. 1991 Nov 29;254(5036):1374-7 PMID: 1962196
  55. Identification of a putative infC-rpmI-rplT operon flanked by long inverted repeats in Mycoplasma fermentans (incognitus strain).
    Gene. 1993 May 15;127(1):79-85 PMID: 8486291
  56. Molecular cloning and sequencing of infC, the gene encoding translation initiation factor IF3, from four enterobacterial species.
    FEMS Microbiol Lett. 1993 Sep 1;112(2):211-6 PMID: 8405963
  57. Mining genomes: correlating tandem mass spectra of modified and unmodified peptides to sequences in nucleotide databases.
    Anal Chem. 1995 Sep 15;67(18):3202-10 PMID: 8686885
  58. Selenocysteine.
    Annu Rev Biochem. 1996;65:83-100 PMID: 8811175
  59. Beta-methylthio-aspartic acid: identification of a novel posttranslational modification in ribosomal protein S12 from Escherichia coli.
    Protein Sci. 1996 Aug;5(8):1625-32 PMID: 8844851
  60. The role of the AUU initiation codon in the negative feedback regulation of the gene for translation initiation factor IF3 in Escherichia coli.
    Mol Microbiol. 1996 Jul;21(2):331-46 PMID: 8858588
  61. Escherichia coli translation initiation factor 3 discriminates the initiation codon in vivo.
    Mol Microbiol. 1996 Jul;21(2):347-60 PMID: 8858589
  62. Identification of oxidized methionine in peptides.
    Rapid Commun Mass Spectrom. 1996;10(15):1905-10 PMID: 9004526
  63. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites.
    Protein Eng. 1997 Jan;10(1):1-6 PMID: 9051728
  64. Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12.
    Electrophoresis. 1997 Aug;18(8):1259-313 PMID: 9298646
  65. Degradative covalent reactions important to protein stability.
    Mol Biotechnol. 1997 Oct;8(2):105-22 PMID: 9406181
  66. Identification of post-translational modifications by blind search of mass spectra.
    Nat Biotechnol. 2005 Dec;23(12):1562-7 PMID: 16311586
  67. GenBank.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D16-20 PMID: 16381837
  68. Interpreting the protein language using proteomics.
    Nat Rev Mol Cell Biol. 2006 Jun;7(6):391-403 PMID: 16723975
  69. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection.
    Mol Syst Biol. 2006;2:2006.0008 PMID: 16738554
  70. Confirmation of the expression of a large set of conserved hypothetical proteins in Shewanella oneidensis MR-1.
    J Microbiol Methods. 2006 Aug;66(2):223-33 PMID: 16417935
  71. Genomic analysis of carbon source metabolism of Shewanella oneidensis MR-1: Predictions versus experiments.
    J Bacteriol. 2006 Jul;188(13):4601-9 PMID: 16788168
  72. Novel gene and gene model detection using a whole genome open reading frame analysis in proteomics.
    Genome Biol. 2006;7(4):R35 PMID: 16646984
  73. A computational approach toward label-free protein quantification using predicted peptide detectability.
    Bioinformatics. 2006 Jul 15;22(14):e481-8 PMID: 16873510
  74. Comparative genomics and experimental characterization of N-acetylglucosamine utilization pathway of Shewanella oneidensis.
    J Biol Chem. 2006 Oct 6;281(40):29872-85 PMID: 16857666
  75. The proteomics of N-terminal methionine cleavage.
    Mol Cell Proteomics. 2006 Dec;5(12):2336-49 PMID: 16963780
  76. Extent of modifications in human proteome samples and their effect on dynamic range of analysis in shotgun proteomics.
    Mol Cell Proteomics. 2006 Dec;5(12):2384-91 PMID: 17015437
  77. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation.
    Nat Biotechnol. 2007 Jan;25(1):117-24 PMID: 17187058
  78. Unrestrictive identification of post-translational modifications through peptide mass spectrometry.
    Nat Protoc. 2006;1(1):67-72 PMID: 17406213
  79. A new UAG-encoded residue in the structure of a methanogen methyltransferase.
    Science. 2002 May 24;296(5572):1462-6 PMID: 12029132
  80. Parallel identification of new genes in Saccharomyces cerevisiae.
    Genome Res. 2002 Aug;12(8):1210-20 PMID: 12176929
  81. The relative rates of glutamine and asparagine deamidation in glucagon fragment 22-29 under acidic conditions.
    J Pharm Sci. 2002 Nov;91(11):2331-45 PMID: 12379918
  82. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis.
    Nat Biotechnol. 2002 Nov;20(11):1118-23 PMID: 12368813
  83. Breathing metals as a way of life: geobiology in action.
    Antonie Van Leeuwenhoek. 2002 Aug;81(1-4):215-22 PMID: 12448720
  84. Signal peptidases.
    Chem Rev. 2002 Dec;102(12):4549-80 PMID: 12475201
  85. RECODE 2003.
    Nucleic Acids Res. 2003 Jan 1;31(1):87-9 PMID: 12519954
  86. Mass spectrometry-based proteomics.
    Nature. 2003 Mar 13;422(6928):198-207 PMID: 12634793
  87. Cyclization of N-terminal S-carbamoylmethylcysteine causing loss of 17 Da from peptides and extra peaks in peptide maps.
    J Proteome Res. 2002 Mar-Apr;1(2):181-7 PMID: 12643538
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
Published
2007-09-00
Epub
2007-00-09
Pages
1362-77
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC1950905
Subset
IM
Grants
NCRR NIH HHS · R01 RR016522 · United States
NCRR NIH HHS · C06 RR017588 · United States
NCRR NIH HHS · P41 RR08605 · United States
NCRR NIH HHS · P41 RR008605 · United States
NCRR NIH HHS · 1-R01-RR16522 · United States
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: product@genelibs.com