Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont.

John P McCutcheon, Bradon R McDonald, Nancy A Moran
Author Information
  1. John P McCutcheon: Center for Insect Science, University of Arizona, Tucson, AZ, USA. jmccutch@email.arizona.edu

Abstract

The genetic code relates nucleotide sequence to amino acid sequence and is shared across all organisms, with the rare exceptions of lineages in which one or a few codons have acquired novel assignments. Recoding of UGA from stop to tryptophan has evolved independently in certain reduced bacterial genomes, including those of the mycoplasmas and some mitochondria. Small genomes typically exhibit low guanine plus cytosine (GC) content, and this bias in base composition has been proposed to drive UGA Stop to Tryptophan (Stop-->Trp) recoding. Using a combination of genome sequencing and high-throughput proteomics, we show that an alpha-Proteobacterial symbiont of cicadas has the unprecedented combination of an extremely small genome (144 kb), a GC-biased base composition (58.4%), and a coding reassignment of UGA Stop-->Trp. Although it is not clear why this tiny genome lacks the low GC content typical of other small bacterial genomes, these observations support a role of genome reduction rather than base composition as a driver of codon reassignment.

References

  1. Appl Environ Microbiol. 2005 Dec;71(12):8802-10 [PMID: 16332876]
  2. J Mol Evol. 1997;44 Suppl 1:S57-64 [PMID: 9395406]
  3. Biochemistry. 1990 Mar 13;29(10):2532-7 [PMID: 2185829]
  4. Proc Natl Acad Sci U S A. 2007 May 15;104 Suppl 1:8627-33 [PMID: 17494762]
  5. Proc Natl Acad Sci U S A. 1987 Jan;84(1):166-9 [PMID: 3467347]
  6. Syst Biol. 2006 Oct;55(5):756-68 [PMID: 17060197]
  7. Nature. 2008 Nov 6;456(7218):53-9 [PMID: 18987734]
  8. J Bacteriol. 1996 Nov;178(21):6192-9 [PMID: 8892818]
  9. Bioinformatics. 2006 Nov 1;22(21):2688-90 [PMID: 16928733]
  10. Proc Natl Acad Sci U S A. 1967 Nov;58(5):1895-902 [PMID: 4866980]
  11. Mol Cell Proteomics. 2005 Sep;4(9):1265-72 [PMID: 15958392]
  12. Mol Biol Evol. 1991 Jul;8(4):530-44 [PMID: 1921708]
  13. J Bacteriol. 1992 Oct;174(20):6321-5 [PMID: 1328155]
  14. J Bacteriol. 2007 Jul;189(13):4578-86 [PMID: 17483224]
  15. Insect Mol Biol. 1995 Feb;4(1):23-9 [PMID: 7538012]
  16. J Mol Evol. 2001 Oct-Nov;53(4-5):299-313 [PMID: 11675590]
  17. J Mol Biol. 1994 Feb 4;235(5):1395-405 [PMID: 8107081]
  18. Microbiol Mol Biol Rev. 1998 Dec;62(4):1094-156 [PMID: 9841667]
  19. Mol Biol Evol. 2005 Mar;22(3):520-32 [PMID: 15525700]
  20. Science. 2001 May 11;292(5519):1096-9 [PMID: 11352062]
  21. J Mol Biol. 1971 Jun 14;58(2):439-58 [PMID: 4933412]
  22. Proc Natl Acad Sci U S A. 1985 Apr;82(8):2306-9 [PMID: 3887399]
  23. Microbiol Rev. 1992 Mar;56(1):229-64 [PMID: 1579111]
  24. J Mol Biol. 1994 Feb 4;235(5):1377-80 [PMID: 8107079]
  25. Proc Natl Acad Sci U S A. 2007 Dec 4;104(49):19392-7 [PMID: 18048332]
  26. Appl Environ Microbiol. 2007 Aug;73(16):5261-7 [PMID: 17586664]
  27. Bioinformatics. 2002 Mar;18(3):502-4 [PMID: 11934758]
  28. J Mol Evol. 1986;24(1-2):39-44 [PMID: 3104617]
  29. Trends Microbiol. 1998 Jul;6(7):263-8 [PMID: 9717214]
  30. Biochem Biophys Res Commun. 2007 Apr 27;356(1):20-5 [PMID: 17336933]
  31. Microb Ecol. 2002 Aug;44(2):137-43 [PMID: 12087426]
  32. Trends Genet. 2002 Jun;18(6):291-4 [PMID: 12044357]
  33. Nat Rev Genet. 2001 Jan;2(1):49-58 [PMID: 11253070]
  34. Curr Biol. 2001 Jan 23;11(2):65-74 [PMID: 11231122]
  35. J Bacteriol. 2001 Mar;183(6):1853-61 [PMID: 11222582]
  36. J Mol Biol. 1966 Aug;19(2):548-55 [PMID: 5969078]
  37. Nature. 1958 Jul 12;182(4628):111-2 [PMID: 13566202]
  38. Nature. 2005 Sep 15;437(7057):376-80 [PMID: 16056220]
  39. Nucleic Acids Res. 2002 Jun 1;30(11):2478-83 [PMID: 12034836]
  40. Nat Biotechnol. 1999 Jul;17(7):676-82 [PMID: 10404161]
  41. J Mol Evol. 2007 Jun;64(6):662-88 [PMID: 17541678]
  42. Science. 2006 Oct 13;314(5797):312-3 [PMID: 17038625]
  43. Annu Rev Genet. 2008;42:165-90 [PMID: 18983256]
  44. Nucleic Acids Res. 1993 Mar 25;21(6):1335-8 [PMID: 8464722]
  45. Proc Natl Acad Sci U S A. 2008 Nov 18;105(46):17878-83 [PMID: 19001264]
  46. J Bacteriol. 1991 Mar;173(5):1810-2 [PMID: 1900283]
  47. Nucleic Acids Res. 2009 Jan;37(Database issue):D141-5 [PMID: 19004872]
  48. Trends Ecol Evol. 2000 Aug;15(8):321-326 [PMID: 10884696]
  49. Science. 2006 Oct 13;314(5797):267 [PMID: 17038615]
  50. Trends Genet. 1988 Jul;4(7):191-8 [PMID: 3070867]
  51. J Mol Biol. 1990 Oct 5;215(3):403-10 [PMID: 2231712]
  52. Nucleic Acids Res. 2005 Jan 20;33(2):511-8 [PMID: 15661851]

Grants

  1. K12 GM000708/NIGMS NIH HHS
  2. 1 K12 GM00708/NIGMS NIH HHS

MeSH Term

Alphaproteobacteria
Animals
Base Composition
Codon, Terminator
Genetic Code
Genome, Bacterial
Hemiptera
Symbiosis
Tryptophan

Chemicals

Codon, Terminator
Tryptophan

Word Cloud

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