Leaderless genes in bacteria: Clue to the evolution of translation initiation mechanisms in prokaryotes

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Zheng, Xiaobin ^a   Hu, Gang Qing ^a,b   She, Zhen Su ^a   Zhu, Huaiqiu ^a  

^a PEKING UNIVERSITY   (China)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOBACTERIA; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; CONTROLLED STUDY; DEINOCOCCUS; GENE SEQUENCE; GENETIC ALGORITHM; LEADERLESS GENE; NONHUMAN; PHYLOGENY; PROKARYOTE; THERMUS; TRANSLATION INITIATION; ALGORITHM; ARCHAEAL GENE; ARCHAEBACTERIUM; BACTERIUM; GENETICS; GENOMICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; REPRODUCIBILITY; RNA TRANSLATION;

ACTINOBACTERIA; ARCHAEA; BACTERIA (MICROORGANISMS); DEINOCOCCUS-THERMUS; PROKARYOTA;

ALGORITHMS; ARCHAEA; BACTERIA; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENES, ARCHAEAL; GENES, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE ANNOTATION; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; REPRODUCIBILITY OF RESULTS;

EID: 79960196885     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-361     Document Type: Article

References (59)

1. Ciccarelli FD, Doerks T, Mering C, Creevey CJ, Snel B, Bork P. Toward Automatic Reconstruction of a Highly Resolved Tree of Life. Science 2006, 311(5765):1283-1287. 10.1126/science.1123061, 16513982.
2. Nakagawa S, Niimura Y, Miura K, Gojobori T. Dynamic evolution of translation initiation mechanisms in prokaryotes. Proc Natl Acad Sci USA 2010, 107(14):6382-6387. 10.1073/pnas.1002036107, 2851962, 20308567.
3. Shine J, Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 1974, 71(4):1342-1346. 10.1073/pnas.71.4.1342, 388224, 4598299.
4. Ptashne M, Backman K, Humayun MZ, Jeffrey A, Maurer R, Meyer B, Sauer RT. Autoregulation and function of a repressor in bacteriophage lambda. Science 1976, 194(4261):156-161. 10.1126/science.959843, 959843.
5. Moll I, Grill S, Gualerzi CO, Blasi U. Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control. Mol Microbiol 2002, 43(1):239-246. 10.1046/j.1365-2958.2002.02739.x, 11849551.
6. Udagawa T, Shimizu Y, Ueda T. Evidence for the translation initiation of leaderless mRNAs by the intact 70 S ribosome without its dissociation into subunits in eubacteria. J Biol Chem 2004, 279(10):8539-8546. 10.1074/jbc.M308784200, 14670970.
7. Grill S, Gualerzi CO, Londei P, Blasi U. Selective stimulation of translation of leaderless mRNA by initiation factor 2: evolutionary implications for translation. Embo J 2000, 19(15):4101-4110. 10.1093/emboj/19.15.4101, 306601, 10921890.
8. Andreev DE, Terenin IM, Dunaevsky YE, Dmitriev SE, Shatsky IN. A leaderless mRNA can bind to mammalian 80S ribosomes and direct polypeptide synthesis in the absence of translation initiation factors. Mol Cell Biol 2006, 26(8):3164-3169. 10.1128/MCB.26.8.3164-3169.2006, 1446950, 16581790.
9. Benelli D, Londei P. Begin at the beginning: evolution of translational initiation. Res Microbiol 2009, 160(7):493-501. 10.1016/j.resmic.2009.06.003, 19576983.
10. Tolstrup N, Sensen CW, Garrett RA, Clausen IG. Two different and highly organized mechanisms of translation initiation in the archaeon Sulfolobus solfataricus. Extremophiles 2000, 4(3):175-179. 10.1007/s007920070032, 10879562.
11. Slupska MM, King AG, Fitz-Gibbon S, Besemer J, Borodovsky M, Miller JH. Leaderless transcripts of the crenarchaeal hyperthermophile Pyrobaculum aerophilum. J Mol Biol 2001, 309(2):347-360. 10.1006/jmbi.2001.4669, 11371158.
12. Torarinsson E, Klenk HP, Garrett RA. Divergent transcriptional and translational signals in Archaea. Environ Microbiol 2005, 7(1):47-54. 10.1111/j.1462-2920.2004.00674.x, 15643935.
13. Brenneis M, Hering O, Lange C, Soppa J. Experimental characterization of Cis-acting elements important for translation and transcription in halophilic archaea. Plos Genet 2007, 3(12):2450-2467.
14. Ma J, Campbell A, Karlin S. Correlations between Shine-Dalgarno sequences and gene features such as predicted expression levels and operon structures. J Bacteriol 2002, 184(20):5733-5745. 10.1128/JB.184.20.5733-5745.2002, 139613, 12270832.
15. Chang B, Halgamuge S, Tang SL. Analysis of SD sequences in completed microbial genomes: Non-SD-led genes are as common as SD-led genes. Gene 2006, 373:90-99.
16. The Translation initiation Signal Database. , http://mech.ctb.pku.edu.cn/leaderless/
17. Shultzaberger RK, Chen Z, Lewis KA, Schneider TD. Anatomy of Escherichia coli sigma70 promoters. Nucleic Acids Res 2007, 35(3):771-788. 10.1093/nar/gkl956, 1807945, 17189297.
18. Wu CJ, Janssen GR. Translation of vph mRNA in Streptomyces lividans and Escherichia coli after removal of the 5' untranslated leader. Mol Microbiol 1996, 22(2):339-355. 10.1046/j.1365-2958.1996.00119.x, 8930918.
19. Ryding NJ, Kelemen GH, Whatling CA, Flardh K, Buttner MJ, Chater KF. A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Mol Microbiol 1998, 29(1):343-357. 10.1046/j.1365-2958.1998.00939.x, 9701826.
20. Nothaft H, Parche S, Kamionka A, Titgemeyer F. In vivo analysis of HPr reveals a fructose-specific phosphotransferase system that confers high-affinity uptake in Streptomyces coelicolor. J Bacteriol 2003, 185(3):929-937. 10.1128/JB.185.3.929-937.2003, 142823, 12533468.
21. Mazurakova V, Sevcikova B, Rezuchova B, Kormanec J. Cascade of sigma factors in streptomycetes: identification of a new extracytoplasmic function sigma factor sigmaJ that is under the control of the stress-response sigma factor sigmaH in Streptomyces coelicolor A3(2). Arch Microbiol 2006, 186(6):435-446. 10.1007/s00203-006-0158-9, 16909271.
22. Ventura M, Canchaya C, Tauch A, Chandra G, Fitzgerald GF, Chater KF, van Sinderen D. Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 2007, 71(3):495-548. 10.1128/MMBR.00005-07, 2168647, 17804669.
23. Janssen GR. Eubacterial, archaebacterial, and eukaryotic genes that encode leaderless mRNA. Industrial Microorganisms: Basic and Applied Molecular Genetics 1993, 59-67. Washington, DC: American Society for Microbiology Press, Baltz RH, Hegeman GD, Skatrud PL.
24. Londei P. Evolution of translational initiation: new insights from the archaea. FEMS Microbiol Rev 2005, 29(2):185-200. 10.1016/j.fmrre.2004.10.002, 15808741.
25. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 2003, 4:41. 10.1186/1471-2105-4-41, 222959, 12969510.
26. Hering O, Brenneis M, Beer J, Suess B, Soppa J. A novel mechanism for translation initiation operates in haloarchaea. Mol Microbiol 2009, 71(6):1451-1463. 10.1111/j.1365-2958.2009.06615.x, 19210623.
27. Sazuka T, Ohara O. Sequence features surrounding the translation initiation sites assigned on the genome sequence of Synechocystis sp. strain PCC6803 by amino-terminal protein sequencing. DNA Res 1996, 3(4):225-232. 10.1093/dnares/3.4.225, 8946162.
28. Kozak M. Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 2005, 361:13-37.
29. Dam P, Olman V, Harris K, Su Z, Xu Y. Operon prediction using both genome-specific and general genomic information. Nucleic Acids Res 2007, 35(1):288-298. 1802555, 17170009.
30. Price MN, Huang KH, Alm EJ, Arkin AP. A novel method for accurate operon predictions in all sequenced prokaryotes. Nucleic Acids Res 2005, 33(3):880-892. 10.1093/nar/gki232, 549399, 15701760.
31. Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A. The Complete Genome Sequence of the Lactic Acid Bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res 2001, 11(5):731-753. 10.1101/gr.GR-1697R, 311110, 11337471.
32. Kaberdina AC, Szaflarski W, Nierhaus KH, Moll I. An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis?. Mol Cell 2009, 33(2):227-236. 10.1016/j.molcel.2008.12.014, 2967816, 19187763.
33. Paget MS, Helmann JD. The sigma70 family of sigma factors. Genome Biol 2003, 4(1):203. 10.1186/gb-2003-4-1-203, 151288, 12540296.
34. Moseley BE, Mattingly A. Repair of irradiation transforming deoxyribonucleic acid in wild type and a radiation-sensitive mutant of Micrococcus radiodurans. J Bacteriol 1971, 105(3):976-983. 248526, 4929286.
35. Henne A, Bruggemann H, Raasch C, Wiezer A, Hartsch T, Liesegang H, Johann A, Lienard T, Gohl O, Martinez-Arias R, et al. The genome sequence of the extreme thermophile Thermus thermophilus. Nat Biotechnol 2004, 22(5):547-553. 10.1038/nbt956, 15064768.
36. Chin K, Shean CS, Gottesman ME. Resistance of Lambda-Ci Translation to Antibiotics That Inhibit Translation Initiation. J Bacteriol 1993, 175(22):7471-7473. 206893, 8226693.
37. Chen H, Bjerknes M, Kumar R, Jay E. Determination of the optimal aligned spacing between the Shine-Dalgarno sequence and the translation initiation codon of Escherichia coli mRNAs. Nucleic Acids Res 1994, 22(23):4953-4957. 10.1093/nar/22.23.4953, 523762, 7528374.
38. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 2007, (35 Database):D61-65.
39. Hu GQ, Zheng XB, Yang YF, Ortet P, She ZS, Zhu HQ. ProTISA: a comprehensive resource for translation initiation site annotation in prokaryotic genomes. Nucleic Acids Res 2008, (36 Database):D114-D119.
40. Hu GQ, Zheng X, Zhu HQ, She ZS. Prediction of translation initiation site for microbial genomes with TriTISA. Bioinformatics 2009, 25(1):123-125. 10.1093/bioinformatics/btn576, 19015130.
41. Zhu HQ, Hu GQ, Yang YF, Wang J, She ZS. MED: a new non-supervised gene prediction algorithm for bacterial and archaeal genomes. BMC Bioinformatics 2007, 8:97. 10.1186/1471-2105-8-97, 1847833, 17367537.
42. Hu GQ, Zheng X, Ju LN, Zhu H, She ZS. Computational evaluation of TIS annotation for prokaryotic genomes. BMC Bioinformatics 2008, 9:160. 10.1186/1471-2105-9-160, 2362131, 18366730.
43. Zhu HQ, Hu GQ, Ouyang ZQ, Wang J, She ZS. Accuracy improvement for identifying translation initiation sites in microbial genomes. Bioinformatics 2004, 20(18):3308-3317. 10.1093/bioinformatics/bth390, 15247104.
44. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 2001, 29(12):2607-2618. 10.1093/nar/29.12.2607, 55746, 11410670.
45. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23(6):673-679. 10.1093/bioinformatics/btm009, 2387122, 17237039.
46. Hershberg R, Bejerano G, Santos-Zavaleta A, Margalit H. PromEC: An updated database of Escherichia coli mRNA promoters with experimentally identified transcriptional start sites. Nucleic Acids Res 2001, 29(1):277. 10.1093/nar/29.1.277, 29777, 11125111.
47. Jiang M, Anderson J, Gillespie J, Mayne M. uShuffle: a useful tool for shuffling biological sequences while preserving the k-let counts. BMC Bioinformatics 2008, 9:192. 10.1186/1471-2105-9-192, 2375906, 18405375.
48. Larkin MA, B G, Brown NP, Chenna R, McGettigan PA, McWilliam H*, Valentin F*, Wallace IM, Wilm A, Lopez R*, Thompson JD, Gibson TJ, Higgins DG. ClustalW and ClustalX version 2. Bioinformatics 2007, 23(21):2947-2948. 10.1093/bioinformatics/btm404, 17846036.
49. Kumar S, Nei M, Dudley J, Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008, 9(4):299-306. 10.1093/bib/bbn017, 2562624, 18417537.
50. Lake JA. Reconstructing evolutionary trees from DNA and protein sequences: paralinear distances. Proc Natl Acad Sci USA 1994, 91(4):1455-1459. 10.1073/pnas.91.4.1455, 43178, 8108430.
51. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190. 10.1101/gr.849004, 419797, 15173120.
52. Anderson TB, Brian P, Champness WC. Genetic and transcriptional analysis of absA, an antibiotic gene cluster-linked two-component system that regulates multiple antibiotics in Streptomyces coelicolor. Mol Microbiol 2001, 39(3):553-566. 10.1046/j.1365-2958.2001.02240.x, 11169098.
53. Hoskisson PA, Rigali S, Fowler K, Findlay KC, Buttner MJ. DevA, a GntR-like transcriptional regulator required for development in Streptomyces coelicolor. J Bacteriol 2006, 188(14):5014-5023. 10.1128/JB.00307-06, 1539961, 16816174.
54. Revill WP, Bibb MJ, Scheu AK, Kieser HJ, Hopwood DA. Beta-ketoacyl acyl carrier protein synthase III (FabH) is essential for fatty acid biosynthesis in Streptomyces coelicolor A3(2). J Bacteriol 2001, 183(11):3526-3530. 10.1128/JB.183.11.3526-3530.2001, 99652, 11344162.
55. Hahn JS, Oh SY, Roe JH. Regulation of the furA and catC operon, encoding a ferric uptake regulator homologue and catalase-peroxidase, respectively, in Streptomyces coelicolor A3(2). J Bacteriol 2000, 182(13):3767-3774. 10.1128/JB.182.13.3767-3774.2000, 94549, 10850993.
56. Umeyama T, Horinouchi S. Autophosphorylation of a bacterial serine/threonine kinase, AfsK, is inhibited by KbpA, an AfsK-binding protein. J Bacteriol 2001, 183(19):5506-5512. 10.1128/JB.183.19.5506-5512.2001, 95440, 11544211.
57. van Wezel GP, White J, Young P, Postma PW, Bibb MJ. Substrate induction and glucose repression of maltose utilization by Streptomyces coelicolor A3(2) is controlled by malR, a member of the lacl-galR family of regulatory genes. Mol Microbiol 1997, 23(3):537-549. 10.1046/j.1365-2958.1997.d01-1878.x, 9044287.
58. Sola-Landa A, Rodriguez-Garcia A, Franco-Dominguez E, Martin JF. Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 2005, 56(5):1373-1385. 10.1111/j.1365-2958.2005.04631.x, 15882427.
59. Hong HJ, Hutchings MI, Neu JM, Wright GD, Paget MS, Buttner MJ. Characterization of an inducible vancomycin resistance system in Streptomyces coelicolor reveals a novel gene (vanK) required for drug resistance. Mol Microbiol 2004, 52(4):1107-1121. 10.1111/j.1365-2958.2004.04032.x, 15130128.