Abstract
The combined set of codon usage frequencies (61 sense codons) from the 111 annotated sequences of leaderless secreted type I, type III, type IV, and type VI proteins from proteobacteria were subjected to the forward and backward selection to obtain a combination of most effective predictor variables for classification/prediction purposes. The group of 24 codon frequencies displayed a strong discriminatory power with an accuracy of 100% for originally grouped and 97.3 ± 1.6% for cross-validated (LOOCV) cases and an acceptable error rate (0.062 ± 0.012) in k-fold (k = 6) cross-validation (KCV). The summary frequencies of synonymous codons for ten amino acids as the alternative predictor variables revealed a comparable discriminatory power (92.8 ± 2.5% for LOOCV), however at somewhat lower levels of prediction accuracy (0.106 ± 0.015 of KCV). A number of significant (p < 0.001) differences were found among indices of codon usage and amino acid composition depending on a definite secretion type. About 60% of secretion substrates were characterized as apparently originated from horizontal gene transfer events or putative alien genes and found to be unequally allocated in respect of groups. The proposed prediction approaches could be used to specify secretome proteins from genomic sequences as well as to assess the compatibility between bacterial secretion pathways and secretion substrates.
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References
Akashi H, Gojobori T (2002) Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc Natl Acad Sci USA 99:3695–700. doi:10.1073/pnas.062526999
Andersone I, Zikmanis P (2007) Distinctive amino acid residue periodicities in terminal sequences of type III and type I secreted proteins from proteobacteria. Central Eur J Biol 2:192–205. doi:10.2478/s11535-007-0017-y
Bendtsen JD, Kiemer L, Fausboll A, Brunak S (2005) Non-classical protein secretion in bacteria. BMC Microbiology 5:58. doi:10.1186/1471-2180-5-58
Cao TB, Saier MH Jr (2001) Conjugal type IV macromolecular transfer systems of Gram-negative bacteria: organismal distribution, structural constraints and evolutionary conclusions. Microbiology 147:3201–3214. doi:10.1016/S0005-2736(02)00662-4
Cascales E, Christie PJ (2003) The versatile bacteria type IV secretion systems. Nat Rev Microbiol 1:137–149. doi:10.1038/nrmicro753
Cochrane G, Akhtar R, Bonfield J, Bower L, Demiralp F, Faruque N, Gibson R, Hoad G, Hubbard T, Hunter C, Jang M, Juhos S, Leinonen R, Leonard S, Lin Q, Lopez R, Lorenc D, McWilliam H, Mukherjee G, Plaister S, Radhakrishnan R, Robinson S, Sobhany S, Hoopen PT, Vaughan R, Zalunin V, Birney E (2008) Petabyte-scale innovations at the European nucleotide archive. Nucleic Acids Res 37(Database issue):D19–D25. doi:10.1093/nar/gkn765
Desvaux M, Hébraud M, Talon R, Henderson IR (2009) Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol 17:139–145. doi:10.1016/j.tim.2009.01.004
Economou A (2002) Bacterial secretome: the assembly manual and operating instructions. Mol Membr Biol 19:159–169. doi:10.1080/09687680210152609
Emmanuelson O, Brunnak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2:953–971. doi:10.1038/nprot.2007.131
Filloux A, Hachani A, Bleves S (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154:1570–1583. doi:10.1099/mic.0.2008/016840-0
Foster PG, Jermiin LS, Hickey AA (1997) Nucleotide comparison bias affects amino acid content in proteins coded by animal mitochondria. J Mol Evol 44:282–288. doi:10.1007/PL00006145
Frank AC, Alsmark CM, Tholleson M, Andersson SGE (2005) Functional divergence and horizontal transfer of the type IV secretion systems. Mol Biol Evol 22:1325–1336. doi:10.1093/molbev/msi124
Garcia-Vallvé S, Romeu A, Palau J (2000) Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res 10:1719–1725. doi:10.1101/gr.130000
Garcia-Vallvé S, Guzman E, Montero MA, Romeu A (2003) HGT-DB: a database of putative horizontally transferred genes in prokaryotic complete genomes. Nucleic Acids Res 31:187–9. doi:10.1093/nar/gkg004, http://www.fut.es/∼debb/HGT/
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acid Res 31:3784–3788. doi:10.1093/nar/gkg563, http://www.expasy.org
Gentschev I, Fensterle J, Schmidt A, Potapenko T, Troppmair J, Goebel W, Rapp UR (2005) Use of a recombinant Salmonella enterica serovar Typhimurium strain expressing C-Raf for protecting against C-raf induced lung adenoma in mice. BMC Cancer 5:15. doi:10.1186/1471-2407-5-15
Gophna U, Ron EZ, Graur D (2003) Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312:151–163. doi:10.1016/S0378-1119(03)00612-7
Grantham R (1974) Amino acid difference formula to help explain protein evolution. Science 185:863–864. doi:10.1126/science.185.4154.862
Holland IB, Schmitt L, Young J (2005) Type 1 protein secretion in bacteria, the ABC-transporter dependent pathway. Mol Membr Biol 22:29–39. doi:10.1080/09687860500042013
Kampenusa I, Zikmanis P (2008) Distinctive attributes for predicted secondary structures at terminal sequences of non-classically secreted proteins from proteobacteria. Central Eur J Biol 3:320–326. doi:10.2478/s11535-008-0026-5
Koonin EV, Aravind L, Kondrashov AS (2000) The impact of comparative genomics on our understanding of evolution. Cell 101:573–576. doi:10.1016/S0092-8674(00)80867-3
Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132. doi:10.1016/0022-2836(82)90515-0
Ma W, Dong FFT, Stavrinides J, Guttman DS (2006) Type III effector diversification via both pathoadaptation and horisontal transfer in response to a coevolutionary arms race. PLoS Genet 2(12):e209. doi:10.1371/journal.pgen.0020209
McCann HC, Guttman DS (2008) Evolution of the type III secetion system and its effectors in plant–microbe interactions. New Phytol 177:33–47. doi:10.1111/j.1469-8137.2007.02293.x
Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, Goodman AL, Joachimiak G, Ordoñez CL, Lory S, Walz T, Joachimiak A, Mekalanos JJ (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526–1530. doi:10.1126/science.1128393
Paila U, Kondam R, Ranjan A (2008) Genome bias influences amino acid choices: analysis of amino acid substitution and re-compilation of substitution matrices exclusive to an AT-biased genome. Nucleic Acids Res 36:6664–6675. doi:10.1093/nar/gkn635
Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 104:15508–15513. doi:10.1073/pnas.0706532104
Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16:276–277. doi:10.1016/S0168-9525(00)02024-2
Rocha EPC, Touchon M, Feil EJ (2006) Similar compositional biases are caused by very different mutational effects. Genome Res 16:1537–1547. doi:10.1101/gr.5525106
Samudrala R, Heffron F, McDermott JE (2009) Accurate prediction of secreted substrates and identification of a conserved putative secretion signal for type III secretion systems. PLoS Pathogens 5:e1000375. doi:10.1371/journal.ppat.1000375
Sharp PM, Li WH (1987) The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295, PMCID: PMC340524
Shrivastava S, Mande SS (2008) Identification and functional characterization of gene components of type VI secretion system in bacteria genomes. PLoS ONE 3(8):e2955. doi:10.1371/journal.pone.0002955
Sobolevsky Y, Trifonov EN (2005) Conserved sequences of prokaryotic proteomes and their compositional age. J Mol Evol 61:591–596. doi:10.1007/s00239-004-0256-8
Sorimachi K, Okayasu T (2008) Codon evolution is governed by linear formulas. Amino Acids 34:661–668. doi:10.1007/s00726-007-0024-3
Stothard P (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28:1102–1104, PMID:10868275 URL: http://www.bioinformatics.org/sms2/rev_trans.html
The UniProt Consortium (2008) The universal protein resource (UniProt). Nucleic Acids Research 36(Database issue):D190–D195. doi:10.1093/nar/gkm895, http://www.uniprot.org
Trifonov EN, Gabdank I, Barash D, Sobolevsky Y (2006) Primordia vita, deconvolution from modern sequences. Orig Life Evol Biosph 36:559–565. doi:10.1007/s11084-006-9042-5
Tseng TT, Tyler BM, Setubal JC (2009) Protein secretion systems in bacterial–host associations and their descrioption in the Gene Onthology. BMC Microbiology 9(Suppl 1):S2. doi:10.1186/1471-2180-9-S1-S2
Vinatzer BA, Jelenska J, Greenberg JT (2005) Bioinformatics correctly identifies many type III secretion substrates in the plant pathogen Pseudomonas syringae and the biocontrol isolate P. fluorescens SBW25. Mol Plant Microbe Interact 18:877–888. doi:10.1094/MPMI-18-0877
Wright F (1990) The 'effective number of codons' used in a gene. Gene 87:23–29. doi:10.1016/0378-1119(90)90491-9
Xia X, Xie Z (2002) Protein structure, neighbor effect, and a new index of amino acid dissimilarities. Mol Biol Evol 19:58–67, ISSN:0737-4038
Zalucki YM, Beacham IR, Jennings MP (2009) Biased codon usage in signal peptides: a role in protein export. Trends Microbiol 17:146–150. doi:10.1016/j.tim.2009.01.005
Zheng J, Leung KY (2007) Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66:1192–1206. doi:10.1111/j.1365-2958.2007.05993.x
Zikmanis P, Andersone I, Baltkalne M (2006) Discriminative features of type I and type III secreted proteins from Gram-negative bacteria. Central Eur J Biol 1:124–136. doi:10.2478/s11535-006-0008-4
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This study was supported by Latvian Council of Science grant 04.1099.
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Kampenusa, I., Zikmanis, P. Distinguishable codon usage and amino acid composition patterns among substrates of leaderless secretory pathways from proteobacteria. Appl Microbiol Biotechnol 86, 285–293 (2010). https://doi.org/10.1007/s00253-009-2423-8
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DOI: https://doi.org/10.1007/s00253-009-2423-8