JZUS - Journal of Zhejiang University SCIENCE

Journal of Zhejiang University SCIENCE B 2010 Vol.11 No.9 P.708-718

Analysis of the 3′ ends of tRNA as the cause of insertion sites of foreign DNA in Prochlorococcus

Author(s): Hai-lan Liu, Jun Zhu
Affiliation(s): Institute of Bioinformatics, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310029, China, Institute of Maize Research, College of Agriculture, Sichuan Agricultural University, Ya’an 625014, China
Corresponding email(s): jzhu@zju.edu.cn
Key Words: Genomic islands, Prochlorococcus, Transfer RNA (tRNA), Palindromic structure, Codon usage

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Abstract: The purpose of this study was to investigate the characteristics of transfer RNA (tRNA) responsible for the association between tRNA genes and genes of apparently foreign origin (genomic islands) in five high-light adapted Prochlorococcus strains. Both bidirectional best BLASTP (basic local alignment search tool for proteins) search and the conservation of gene order against each other were utilized to identify genomic islands, and 7 genomic islands were found to be immediately adjacent to tRNAs in Prochlorococcus marinus AS9601, 11 in P. marinus MIT9515, 8 in P. marinus MED4, 6 in P. marinus MIT9301, and 6 in P. marinus MIT9312. Monte Carlo simulation showed that tRNA genes are hotspots for the integration of genomic islands in Prochlorococcus strains. The tRNA genes associated with genomic islands showed the following characteristics: (1) the association was biased towards a specific subset of all iso-accepting tRNA genes; (2) the codon usages of genes within genomic islands appear to be unrelated to the codons recognized by associated tRNAs; and, (3) the majority of the 3’ ends of associated tRNAs lack CCA ends. These findings contradict previous hypotheses concerning the molecular basis for the frequent use of tRNA as the insertion site for foreign genetic materials. The analysis of a genomic island associated with a tRNA-Asn gene in P. marinus MIT9301 suggests that foreign genetic material is inserted into the host genomes by means of site-specific recombination, with the 3’ end of the tRNA as the target, and during the process, a direct repeat of the 3’ end sequence of a boundary tRNA (namely, a scar from the process of insertion) is formed elsewhere in the genomic island. Through the analysis of the sequences of these targets, it can be concluded that a region characterized by both high GC content and a palindromic structure is the preferred insertion site.

Reference

[1]Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25(17):3389-3402.

[2]Baar, C., Eppinger, M., Raddatz, G., Simon, J., Lanz, C., Klimmer, O., Nandakumar, R., Cross, R., Rosinus, A., Keller, H., et al., 2003. Complete genome sequence and analysis of Wolinella succinogenes. PNAS, 100(20):11690-11695.

[3]Boto, L., 2010. Horizontal gene transfer in evolution: facts and challenges. Proc. R. Soc. B, 277(1683):819-827.

[4]Cheetham, B.F., Katz, M.E., 1995. A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol. Microbiol., 18(2):201-208.

[5]Choi, I.G., Kim, S.H., 2007. Global extent of horizontal gene transfer. PNAS, 104(11):4489-4494.

[6]Coleman, M.L., Sullivan, M.B., Martiny, A.C., Steglich, C., Barry, K., Delong, E.F., Chisholm, S.W., 2006. Genomic islands and the ecology and evolution of Prochlorococcus. Science, 311(5768):1768-1770.

[7]Elhai, J., Taton, A., Massar, J.P., Myers, J.K., Travers, M., Casey, J., Slupesky, M., Shrager, J., 2009. BioBIKE: a Web-based, programmable, integrated biological knowledge base. Nucleic Acids Res., 37(web server):W28-W32.

[8]Garcia-Vallvé, V.S., Romeu, A., Palau, J., 2000. Horizontal gene transfer in bacterial and archaeal complete genomes. Genome Res., 10(11):1719-1725.

[9]Hacker, J., Carniel, E., 2001. Ecological fitness, genomic islands and bacterial pathogenicity. EMBO Rep., 2(5):376-381.

[10]Hess, W.R., Rocap, G., Ting, C.S., Larimer, F., Stilwagen, S., Lamerdin, J., Chisholm, S.W., 2001. The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynth. Res., 70(1):53-71.

[11]Hou, Y.M., 1999. Transfer RNAs and pathogenicity islands. Trends Biochem. Sci., 24(8):295-298.

[12]Hsiao, W., Wan, I., Jones, S.J., Brinkman, F.S.L., 2003. IslandPath: aiding detection of genomic islands in prokaryotes. Bioinformatics, 19(3):418-420.

[13]Kettler, G.C., Martiny, A.C., Huang, K., Zuker, J., Coleman, M.L., Rodrigue, S., Chen, F., Lapidus, A., Ferriera, S., Johnson, J., et al., 2007. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet., 3(12):e231.

[14]Koonin, E.V., 2009. Darwinian evolution in the light of genomics. Nucleic Acids Res., 37(4):1011-1034.

[15]Koonin, E.V., Makarova, K.S., Aravind, L., 2001. Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol., 55(1):709-742.

[16]Liu, H.L., Zhu, J., 2010. Identification of genomic islands in the genomes of five Prochlorococcus strains by multiple genomic comparison. J. Zhejiang Univ. (Agric. & Life Sci.), 36(5):473-484.

[17]Nakamura, Y., Itoh, T., Matsuda, H., Gojobori, T., 2004. Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat. Genet., 36(7):760-766.

[18]Nelson, K.E., Clayton, R.A., Gill, S.R., Gwinn, M.L., Dodson, R.J., Haft, D.H., Hickey, E.K., Peterson, J.D., Nelson, W.C., Ketchum, K.A., et al., 1999. Evidence for lateral gene transfer between archaea and bacteria from genome sequence of Thermotoga maritime. Nature, 399(6734):323-329.

[19]Parreira, V.R., Gyles, C.L., 2003. A novel pathogenicity island integrated adjacent to the thrW tRNA gene of avian pathogenic Escherichia coli encodes a vacuolating autotransporter toxin. Infect. Immun., 71(9):5087-5096.

[20]Partensky, F., Hess, W.R., Vaulot, D., 1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev., 63(1):106-127.

[21]Reiter, W.D., Palm, P., Yeats, S., 1989. Transfer RNA genes frequently serve as integration sites for prokaryotic genetic elements. Nucleic Acids Res., 17(5):1907-1914.

[22]Ritter, A., Blum, G., Emody, L., Kerenyi, M., Bock, A., Neuhieri, B., Rabsch, W., Scheutz, F., Hacker, J., 1995. tRNA genes and pathogenicity islands: influence on virulence and metabolic properties of uropathogenic Escherichia coli. Mol. Microbiol., l7(1):109-121.

[23]Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., Arellano, A., Coleman, M., Hauser, L., Hess, W.R., et al., 2003. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424(6952):1042-1047.

[24]Semsey, S., Blaha, B., Koles, K., Orosz, L., Papp, P.P., 2002. Site-specific integrative elements of rhizobiophage 16-3 can integrate into proline tRNA (CGG) genes in different bacterial genera. J. Bacteriol., 184(1):177-182.

[25]Syvanen, M., 1994. Horizontal gene transfer: evidence and possible consequences. Annu. Rev. Genet., 28(1):237-261.

[26]Tamura, K., Dudley, J., Nei, M., Kumar, S., 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol., 24(8):1596-1599.

[27]Tian, Y.J., Yang, H., Wu, X.J., Li, D.T., 2005. Molecular analysis of microbial community in a groundwater sample polluted by landfill leachate and seawater. J. Zhejiang Univ.-Sci. B, 6(3):165-170.

[28]Tuanyok, A., Leadem, B.R., Auerbach, R.K., Beckstrom-Sternberg, S.M., Beckstrom-Sternberg, J.S., Mayo, M., Wuthiekanum, V., Brettin, T.S., Nierman, W.C., Peacock, S.J., et al., 2008. Genomic islands from five strains of Burkholderia pseudomallei. BMC Genomics, 9(1):566.

[29]van Aartsen, J.J., 2008. The Klebsiella pheV tRNA locus: a hotspot for integration of alien genomic islands. Biosci. Horiz., 1(1):51-60.

[30]Wang, X.S., Zhu, J., Mansueto, L., Bruskiewich, R., 2005. Identification of candidate genes for drought strees tolerance in rice by the integration of a genetic (QTL) map with the rice genome physical map. J. Zhejiang Univ.-Sci. B, 6(5):382-388.

[31]Williams, K.P., 2002. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic. Acids Res., 30(4):866-875.

[32]Xu, X.Z., Liu, Q.B., Fan, L.J., Cui, X.F., Zhou, X.P., 2008. Analysis of synonymous codon usage and evolution of begomoviruses. J. Zhejiang Univ.-Sci. B, 9(9):667-674.

[33]Zhaxybayeva, O., Gogarten, J.P., Charlebois, R.L., Doolittle, W.F., Papke, R.T., 2006. Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res., 16(9):1099-1108.

[34]Zinser, E.R., Johnson, Z.I., Coe, A., Karaca, E., Veneziano, D., Chisholm, S.W., 2007. Influence of light and temperature on Prochlorococcus ecotype distributions in the Atlantic Ocean. Limnol. Oceanogr., 52(5):2205-2220.

[35]Zuker, M., 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic. Acids Res., 31(13):3406-3415.

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