OpenLB
Open Library of Bioscience
Advanced Search
Microbiology spectrum
07, 2018;6 (4):

Genes within Genes in Bacterial Genomes.

Sezen Meydan, Nora Vázquez-Laslop, Alexander S Mankin
Author Information
  1. Sezen Meydan: Center for Biomolecular Sciences, University of Illinois at Chicago, Chicago, IL 60607.
  2. Nora Vázquez-Laslop: Center for Biomolecular Sciences, University of Illinois at Chicago, Chicago, IL 60607.
  3. Alexander S Mankin: Center for Biomolecular Sciences, University of Illinois at Chicago, Chicago, IL 60607.
PMID: 30003865 DOI: 10.1128/microbiolspec.RWR-0020-2018

Abstract

Genetic coding in bacteria largely operates via the "one gene-one protein" paradigm. However, the peculiarities of the mRNA structure, the versatility of the genetic code, and the dynamic nature of translation sometimes allow organisms to deviate from the standard rules of protein encoding. Bacteria can use several unorthodox modes of translation to express more than one protein from a single mRNA cistron. One such alternative path is the use of additional translation initiation sites within the gene. Proteins whose translation is initiated at different start sites within the same reading frame will differ in their N termini but will have identical C-terminal segments. On the other hand, alternative initiation of translation in a register different from the frame dictated by the primary start codon will yield a protein whose sequence is entirely different from the one encoded in the main frame. The use of internal mRNA codons as translation start sites is controlled by the nucleotide sequence and the mRNA folding. The proteins of the alternative proteome generated via the "genes-within-genes" strategy may carry important functions. In this review, we summarize the currently known examples of bacterial genes encoding more than one protein due to the utilization of additional translation start sites and discuss the known or proposed functions of the alternative polypeptides in relation to the main protein product of the gene. We also discuss recent proteome- and genome-wide approaches that will allow the discovery of novel translation initiation sites in a systematic fashion.

References

  1. Nature. 2000 Feb 3;403(6769):571-5 [PMID: 10676969]
  2. Nat Microbiol. 2017 Feb 13;2:17005 [PMID: 28191904]
  3. J Bacteriol. 1987 Oct;169(10):4602-7 [PMID: 3115961]
  4. Nature. 1975 Mar 6;254(5495):34-8 [PMID: 803646]
  5. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7787-91 [PMID: 6096856]
  6. J Bacteriol. 1997 Jan;179(1):287-9 [PMID: 8982012]
  7. J Bacteriol. 1987 Jun;169(6):2466-70 [PMID: 3034857]
  8. Nucleic Acids Res. 1986 Jun 11;14(11):4453-69 [PMID: 3520485]
  9. Mol Microbiol. 2011 Sep;81(5):1178-89 [PMID: 21790803]
  10. J Biol Chem. 1973 Feb 10;248(3):1084-90 [PMID: 4567787]
  11. Mol Microbiol. 2002 Jan;43(1):239-46 [PMID: 11849551]
  12. Curr Opin Struct Biol. 2014 Apr;25:111-7 [PMID: 24704748]
  13. Arch Biochem Biophys. 2012 Mar 15;519(2):186-93 [PMID: 22079167]
  14. J Mol Biol. 2010 Feb 26;396(3):697-707 [PMID: 19961856]
  15. EMBO Rep. 2003 Jan;4(1):37-41 [PMID: 12524518]
  16. RNA. 2004 Sep;10(9):1359-65 [PMID: 15317973]
  17. J Bacteriol. 1996 Aug;178(16):4839-46 [PMID: 8759846]
  18. Microbiol Mol Biol Rev. 2016 Jun 15;80(3):597-628 [PMID: 27307578]
  19. Proc Natl Acad Sci U S A. 2006 Nov 28;103(48):18368-73 [PMID: 17116880]
  20. J Biol Chem. 2002 Dec 6;277(49):47160-6 [PMID: 12351638]
  21. J Bacteriol. 2015 Jan 1;197(1):18-28 [PMID: 25266388]
  22. Mol Microbiol. 1992 May;6(9):1105-14 [PMID: 1375309]
  23. Mol Gen Genet. 1995 Apr 10;247(1):73-85 [PMID: 7536296]
  24. Genome Res. 2012 Nov;22(11):2208-18 [PMID: 22879431]
  25. RNA. 2004 Feb;10(2):265-76 [PMID: 14730025]
  26. J Biol Chem. 2011 Oct 14;286(41):36098-36107 [PMID: 21878641]
  27. Plasmid. 2014 Nov;76:72-8 [PMID: 25454070]
  28. Microbiol Mol Biol Rev. 2013 Sep;77(3):357-79 [PMID: 24006469]
  29. Gene. 2005 Nov 21;361:13-37 [PMID: 16213112]
  30. J Mol Biol. 2009 Feb 6;385(5):1361-74 [PMID: 19109978]
  31. Infect Immun. 1997 Jul;65(7):2904-13 [PMID: 9199466]
  32. Nucleic Acids Res. 2016 Sep 6;44(15):7007-78 [PMID: 27436286]
  33. PLoS One. 2011;6(8):e22914 [PMID: 21857964]
  34. Biochem Biophys Res Commun. 1991 Dec 31;181(3):1572-9 [PMID: 1764105]
  35. Protein Expr Purif. 1993 Dec;4(6):512-8 [PMID: 8286947]
  36. ACS Synth Biol. 2015 Mar 20;4(3):249-57 [PMID: 24931615]
  37. Biochemistry. 2012 Feb 28;51(8):1669-77 [PMID: 22320351]
  38. J Bacteriol. 1991 Sep;173(18):5861-8 [PMID: 1885553]
  39. Biochem Biophys Res Commun. 1982 Apr 29;105(4):1546-53 [PMID: 7049165]
  40. J Bacteriol. 1991 Sep;173(18):5740-6 [PMID: 1885547]
  41. J Biol Chem. 1988 Jul 5;263(19):9526-32 [PMID: 2837491]
  42. Microbiol Mol Biol Rev. 2009 Dec;73(4):594-651 [PMID: 19946135]
  43. Methods Enzymol. 2011;498:19-42 [PMID: 21601672]
  44. Mol Microbiol. 1991 May;5(5):1197-204 [PMID: 1956296]
  45. EMBO J. 1985 Jan;4(1):223-9 [PMID: 3894004]
  46. J Bacteriol. 1995 Nov;177(22):6560-7 [PMID: 7592434]
  47. Cell. 2011 Nov 11;147(4):789-802 [PMID: 22056041]
  48. Mol Microbiol. 2014 Apr;92(1):28-46 [PMID: 24612328]
  49. Nat Rev Microbiol. 2015 Sep;13(9):559-72 [PMID: 26256789]
  50. J Bacteriol. 1990 Mar;172(3):1312-20 [PMID: 2307650]
  51. J Mol Biol. 1984 May 25;175(3):229-49 [PMID: 6327994]
  52. Biochemistry. 2018 Jan 9;57(1):56-60 [PMID: 29039649]
  53. Plasmid. 1987 Sep;18(2):164-9 [PMID: 2829253]
  54. J Biol Chem. 2003 Nov 14;278(46):45305-10 [PMID: 12952979]
  55. Mol Microbiol. 1992 Mar;6(5):629-34 [PMID: 1552862]
  56. Science. 2009 Apr 10;324(5924):218-23 [PMID: 19213877]
  57. Nat Rev Genet. 2015 Sep;16(9):517-29 [PMID: 26260261]
  58. J Mol Biol. 1984 May 25;175(3):251-62 [PMID: 6374158]
  59. J Bacteriol. 1994 Jan;176(1):189-97 [PMID: 8282695]
  60. DNA Res. 2016 Jun;23(3):193-201 [PMID: 27013550]
  61. PLoS Genet. 2012;8(4):e1002648 [PMID: 22536160]
  62. Bioorg Med Chem. 2009 Mar 15;17(6):2137-46 [PMID: 19027305]
  63. Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4291-6 [PMID: 17360517]
  64. Nat Struct Mol Biol. 2017 Sep;24(9):752-757 [PMID: 28741611]
  65. J Biol Chem. 2010 Aug 27;285(35):27477-27486 [PMID: 20573952]
  66. Cell Mol Life Sci. 2015 Nov;72(22):4341-67 [PMID: 26259514]
  67. Philos Trans R Soc Lond B Biol Sci. 2017 Mar 19;372(1716): [PMID: 28138069]
  68. Biochem Biophys Res Commun. 2004 Jan 9;313(2):294-9 [PMID: 14684159]
  69. Biochem J. 1998 Oct 1;335 ( Pt 1):67-77 [PMID: 9742214]
  70. Mol Gen Genet. 1985;201(3):529-36 [PMID: 3003543]
  71. Biochim Biophys Acta. 2014 Aug;1843(8):1629-41 [PMID: 24129268]
  72. PLoS Genet. 2014 Jul 31;10(7):e1004463 [PMID: 25078267]
  73. J Bacteriol. 1998 Jun;180(11):2936-42 [PMID: 9603885]
  74. J Bacteriol. 2001 Mar;183(6):2032-40 [PMID: 11222602]
  75. J Biol Chem. 1993 Sep 25;268(27):20170-4 [PMID: 8376377]
  76. FEMS Microbiol Lett. 2001 Nov 13;204(2):259-63 [PMID: 11731132]
  77. J Biol Chem. 1994 Nov 25;269(47):29468-73 [PMID: 7961929]
  78. Adv Exp Med Biol. 2008;631:54-79 [PMID: 18792682]
  79. Nat Prod Rep. 2012 Feb;29(2):264-325 [PMID: 22186970]
  80. J Biol Chem. 1985 Jan 10;260(1):592-7 [PMID: 2981222]
  81. Nucleic Acids Res. 2017 Sep 19;45(16):9573-9582 [PMID: 28934499]
  82. Microbiol Mol Biol Rev. 2003 Mar;67(1):86-156, table of contents [PMID: 12626685]
  83. J Mol Biol. 2006 Sep 29;362(4):787-99 [PMID: 16935296]
  84. Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:111-140 [PMID: 15012188]
  85. Microbiol Spectr. 2018 Apr;6(2): [PMID: 29623874]
  86. J Bacteriol. 1985 Jul;163(1):94-105 [PMID: 3891743]
  87. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5370-4 [PMID: 6449010]
  88. Nat Commun. 2017 May 09;8:14737 [PMID: 28485369]
  89. Plant Physiol. 2010 May;153(1):285-93 [PMID: 20304968]
  90. Microbiology (Reading). 2014 Apr;160(Pt 4):789-794 [PMID: 24464800]
  91. Proteomics. 2016 Jan;16(2):257-72 [PMID: 26442651]
  92. J Biol Chem. 2007 Oct 5;282(40):29323-35 [PMID: 17675289]
  93. J Bacteriol. 1990 Jan;172(1):511-3 [PMID: 2294096]
  94. Proc Natl Acad Sci U S A. 2012 Sep 11;109(37):E2424-32 [PMID: 22927429]
  95. J Bacteriol. 1987 Mar;169(3):1239-45 [PMID: 3029027]
  96. Genes Cells. 2002 Sep;7(9):901-10 [PMID: 12296821]
  97. Eur J Biochem. 1985 Mar 1;147(2):437-46 [PMID: 3882429]
  98. Mol Genet Genomics. 2002 Jan;266(5):873-81 [PMID: 11810263]
  99. Mol Biol Evol. 2014 Jun;31(6):1421-31 [PMID: 24600050]
  100. J Bacteriol. 1991 Mar;173(6):2116-9 [PMID: 2002011]
  101. J Mol Biol. 2008 Feb 1;375(5):1212-21 [PMID: 18076902]
  102. Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5455-60 [PMID: 12704232]
  103. J Bacteriol. 1997 Dec;179(24):7768-75 [PMID: 9401036]
  104. EMBO J. 1998 Sep 15;17(18):5477-83 [PMID: 9736625]
  105. Wiley Interdiscip Rev RNA. 2012 Sep-Oct;3(5):661-73 [PMID: 22715123]
  106. FEBS Lett. 2005 Aug 15;579(20):4235-41 [PMID: 16038902]
  107. J Bacteriol. 1989 Apr;171(4):1974-81 [PMID: 2649480]
  108. Mol Gen Genet. 1984;196(3):449-57 [PMID: 6094972]
  109. J Bacteriol. 2000 Dec;182(24):7092-6 [PMID: 11092876]
  110. Mol Microbiol. 1995 Jan;15(1):55-63 [PMID: 7752896]
  111. J Bacteriol. 1994 Jan;176(1):256-9 [PMID: 8282705]
  112. Antimicrob Agents Chemother. 2006 Nov;50(11):3875-81 [PMID: 16940066]
  113. Mol Genet Genomics. 2004 Jan;270(6):533-8 [PMID: 14618393]
  114. Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1389-93 [PMID: 1996339]
  115. J Bacteriol. 1997 Feb;179(3):689-96 [PMID: 9006022]
  116. Cell. 2014 Apr 24;157(3):624-35 [PMID: 24766808]
  117. Biochemistry. 2002 Apr 23;41(16):5245-54 [PMID: 11955074]
  118. Proteomics. 2015 Jul;15(14):2503-18 [PMID: 26017780]
  119. J Mol Biol. 1992 May 5;225(1):67-80 [PMID: 1374802]
  120. Trends Biochem Sci. 2015 May;40(5):265-74 [PMID: 25850333]
  121. Electrophoresis. 1998 Apr;19(4):515-27 [PMID: 9588797]
  122. J Bacteriol. 1991 Jul;173(14):4254-62 [PMID: 2066329]
  123. Mol Biol (Mosk). 2000 Jul-Aug;34(4):572-83 [PMID: 11042850]
  124. Nat Rev Mol Cell Biol. 2013 Oct;14(10):617-29 [PMID: 24061228]
  125. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9397-401 [PMID: 7937777]
  126. Microbiology (Reading). 2003 Jan;149(Pt 1):9-17 [PMID: 12576575]
  127. Biochim Biophys Acta. 2015 Oct;1850(10):2096-102 [PMID: 25529296]
  128. Mol Microbiol. 2016 Feb;99(4):749-66 [PMID: 26538516]
  129. Microbiol Mol Biol Rev. 2005 Mar;69(1):101-23 [PMID: 15755955]
  130. J Biochem. 2014 Jan;155(1):5-16 [PMID: 24001521]
  131. Proc Natl Acad Sci U S A. 2003 May 13;100(10):5724-9 [PMID: 12719542]
  132. Trends Biochem Sci. 2006 Jun;31(6):333-41 [PMID: 16679018]
  133. Nucleic Acids Res. 2014 Jan;42(1):56-69 [PMID: 23990325]
  134. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1518-22 [PMID: 8434013]
  135. J Antibiot (Tokyo). 1992 Dec;45(12):1981-2 [PMID: 1490892]
  136. Nucleic Acids Res. 2013 Jan 7;41(1):474-86 [PMID: 23093605]
  137. FEBS Lett. 1995 Dec 11;377(1):41-3 [PMID: 8543014]
  138. J Bacteriol. 1990 May;172(5):2675-87 [PMID: 2110148]
  139. Mol Microbiol. 2007 Dec;66(6):1566-78 [PMID: 18028309]

MeSH Term

Bacteria
Bacterial Proteins
Codon, Initiator
Gene Expression Regulation, Bacterial
Genes, Overlapping
Genetic Code
Genome, Bacterial
Open Reading Frames
Peptide Chain Initiation, Translational

Chemicals

Bacterial Proteins
Codon, Initiator
Journal Article Research Support, U.S. Gov't, Non-P.H.S. Review
Article has an altmetric score of 1

Word Cloud

Created with Highcharts 10.0.0translationproteinsitesmRNAalternativestartwilluseoneinitiationwithindifferentframeviaallowencodingadditionalgenewhosesequencemainfunctionsknowndiscussGenesGeneticcodingbacterialargelyoperates"onegene-oneprotein"paradigmHoweverpeculiaritiesstructureversatilitygeneticcodedynamicnaturesometimesorganismsdeviatestandardrulesBacteriacanseveralunorthodoxmodesexpresssinglecistronOnepathProteinsinitiatedreadingdifferNterminiidenticalC-terminalsegmentshandregisterdictatedprimarycodonyieldentirelyencodedinternalcodonscontrollednucleotidefoldingproteinsproteomegenerated"genes-within-genes"strategymaycarryimportantreviewsummarizecurrentlyexamplesbacterialgenesdueutilizationproposedpolypeptidesrelationproductalsorecentproteome-genome-wideapproachesdiscoverynovelsystematicfashionBacterialGenomes

Similar Articles

Cited By