Advertisement

Origins of Life and Evolution of Biospheres

, Volume 43, Issue 4–5, pp 363–375 | Cite as

Norvaline and Norleucine May Have Been More Abundant Protein Components during Early Stages of Cell Evolution

  • Claudia Alvarez-Carreño
  • Arturo Becerra
  • Antonio Lazcano
Protein Evolution

Abstract

The absence of the hydrophobic norvaline and norleucine in the inventory of protein amino acids is readdressed. The well-documented intracellular accumulation of these two amino acids results from the low-substrate specificity of the branched-chain amino acid biosynthetic enzymes that act over a number of related α-ketoacids. The lack of absolute substrate specificity of leucyl-tRNA synthase leads to a mischarged norvalyl-tRNALeu that evades the translational proofreading activites and produces norvaline-containing proteins, (cf. Apostol et al. J Biol Chem 272:28980–28988, 1997). A similar situation explains the presence of minute but detectable amounts of norleucine in place of methionine. Since with few exceptions both leucine and methionine are rarely found in the catalytic sites of most enzymes, their substitution by norvaline and norleucine, respectively, would have not been strongly hindered in small structurally simple catalytic polypeptides during the early stages of biological evolution. The report that down-shifts of free oxygen lead to high levels of intracellular accumulation of pyruvate and the subsequent biosynthesis of norvaline (Soini et al. Microb Cell Factories 7:30, 2008) demonstrates the biochemical and metabolic consequences of the development of a highly oxidizing environment. The results discussed here also suggest that a broader definition of biomarkers in the search for extraterrestrial life may be required.

Keywords

Norvaline Norleucine Prebiotic amino acids Misincorporation of norvaline and norleucine in proteins Aminoacyl-tRNA synthases 

Notes

Acknowledgments

Support of the Posgrado en Ciencias Biomédicas, UNAM, to CAC is gratefully acknowledged. We are indebted to an anonymous reviewer for many kind suggestions. Part of the work reported here was completed during a sabbatical leave of absence of AB, with support of DGAPA-UNAM, where he enjoyed the hospitality of Professor Juli Peretó at the Instituto Cavanilles (Valencia, Spain).

References

  1. Anfinsen C, Corley L (1969) An active variant of staphylococcal nuclease containing norleucine in place of methionine. J Biol Chem 244:5149–5152PubMedGoogle Scholar
  2. Apostol I, Levine J, Lippincott J et al (1997) Incorporation of norvaline at leucine positions in recombinant human hemoglobin expressed in Escherichia coli. J Biol Chem 272:28980–28988PubMedCrossRefGoogle Scholar
  3. Bada JL (2001) State-of-the-art instruments for detecting extraterrestrial life. Proc Natl Acad Sci U S A 98:707–800CrossRefGoogle Scholar
  4. Barker DG, Bruton CJ (1979) The fate of norleucine as a replacement for methionine in protein synthesis. J Mol Biol 133:217–231PubMedCrossRefGoogle Scholar
  5. Bogosian G, Violand BN, Dorward-King EJ et al (1989) Biosynthesis and incorporation into protein of norleucine by Escherichia coli. J Biol Chem 264:531–539PubMedGoogle Scholar
  6. Brown J, Doolittle W (1995) Root of the universal tree of life based on ancient aminoacyl-tRNA synthase gene duplications. Proc Natl Acad Sci U S A 92:2441–2445PubMedCentralPubMedCrossRefGoogle Scholar
  7. Budisa N (2004) Prolegomena to future experimental efforts on genetic code engineering by expanding its amino acid repertoire. Angew Chem Int Ed 43:6426–6463CrossRefGoogle Scholar
  8. Burton AS, Stern JC, Elsila JE et al (2012) Understanding prebiotic chemistry through the analysis of extraterrestrial amino acids and nucleobases in meteorites. Chem Soc Rev 41:5459–5472PubMedCrossRefGoogle Scholar
  9. Cleaves HJ (2010) The origin of the biologically coded amino acids. J Theor Biol 263:490–498PubMedCrossRefGoogle Scholar
  10. Cleaves HJ (2012) Prebiotic chemistry: what we know, what we don’t. Evol Educ Outreach 5:342–360CrossRefGoogle Scholar
  11. Cohen GN, Munier R (1959) Effects of structural analogues of amino acids on growth and synthesis of proteins and enzymes in Escherichia coli. Biochim Biophys Acta 31:347–356PubMedCrossRefGoogle Scholar
  12. Cowie DB, Cohen GN, Bolton ET, De Robichon-Szulmajster H (1959) Amino acid analog incorporation into bacterial proteins. Biochim Biophys Acta 34:39–46PubMedCrossRefGoogle Scholar
  13. Cusack S, Yaremchuk A, Tukalo M (2000) The 2 Å crystal structure of leucyl-tRNA synthetase and its complex with a leucyl-adenylate analogue. EMBO J 19:2351–2361PubMedCentralPubMedCrossRefGoogle Scholar
  14. Cvetesic N, Akmacic I, Gruic-Sovulj I (2013) Lack of discrimination against non-proteinogenic amino acid norvaline by elongation factor Tu from Escherichia coli. Croat Chem Acta 86:73–82PubMedCentralPubMedCrossRefGoogle Scholar
  15. Deckert G, Warren PV, Gaasterland T et al (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392:353–358PubMedCrossRefGoogle Scholar
  16. Döring V, Mootz HD, Nangle LA et al (2001) Enlarging the amino acid set of Escherichia coli by infiltration of the valine coding pathway. Science 292:501–504PubMedCrossRefGoogle Scholar
  17. EMBL-EBI (2013) Query MACiE Reactions by Amino Acid Residue. http://www.ebi.ac.uk/thornton-srv/databases/MACiE/queryMACiE.html. Accessed 21 June 2013
  18. Holliday GL, Almonacid DE, Mitchell JBO, Thorton JM (2007) The chemistry of protein catalysis. J Mol Biol 372:1261–1277PubMedCrossRefGoogle Scholar
  19. Holliday GL, Mitchell JBO, Thornton JM (2009) Understanding the functional roles of amino acid residues in enzyme catalysis. J Mol Biol 390:560–577PubMedCrossRefGoogle Scholar
  20. Johnson AP, Cleaves HJ, Dworkin JP et al (2008) The Miller volcanic spark discharge experiment. Science 322:404PubMedCrossRefGoogle Scholar
  21. Kanehisa Laboratories (2012) KEGG: Kyoto encyclopedia of genes and genomes. http://www.genome.jp/kegg/. Accessed 21 June 2013
  22. Kepner RE, Castor JGB, Webb AD (1954) Conversion of α-amino-n-butyric acid to n-propanol during alcoholic fermentation. Arch Biochem Biophys 51:88–93PubMedCrossRefGoogle Scholar
  23. Kisumi M, Sugiura M, Chibata I (1976) Biosynthesis of norvaline, norleucine, and homoisoleucine in Serratia marcescens. J Biochem 80:333–339PubMedGoogle Scholar
  24. Lazcano A (2012) Planetary change and biochemical adaptation: molecular evolution of corrinoid and heme biosynthesis. Hematol Suppl 1:S7–S10Google Scholar
  25. Liu CC, Schultz PG (2010) Adding new chemistries to the genetic code. Annu Rev Biochem 79:413–444PubMedCrossRefGoogle Scholar
  26. Lu Y, Freeland SJ (2008) A quantitative investigaction of the chemical space surrounding amino acid alphabet formation. J Theor Biol 250:349–361PubMedCrossRefGoogle Scholar
  27. Lyu PC, Sherman A, Kallenbach NR (1991) α-Helix stabilization by natural and unnatural amino acids with alkyl side-chains. Proc Natl Acad Sci U S A 88:5317–5320PubMedCentralPubMedCrossRefGoogle Scholar
  28. McDonald A (2013) ExplorEnz—the enzyme database. In: International Union of Biochemistry and Molecular Biology. http://www.enzyme-database.org/. Accessed 26 June 2013
  29. McDonald GD, Storrie-Lombardi MC (2010) Biochemical constraints in a protobiotic earth devoid of basic amino acids: the “BAA(−) world”. Astrobiology 10:989–1000PubMedCrossRefGoogle Scholar
  30. Munier R, Cohen GN (1959) Incorporation of structural analogues of amino acids into bacterial proteins during their synthesis in vivo. Biochim Biophys Acta 31:378–391PubMedCrossRefGoogle Scholar
  31. Nandi P, Sen GP (1953) An antifungal substance from a strain of B subtilis. Nature 172:871–872PubMedCrossRefGoogle Scholar
  32. Old JM, Jones DS (1975) The recognition of methionine analogues by Escherichia coli methionyl-transfer ribonucleic acid synthetase. Biochem Soc Trans 3:659–660PubMedGoogle Scholar
  33. Orgel LE, Sulston JE (1971) Polynucleotide replication and the origin of life. In: Kimball AP, Oró J (eds) Prebiotic and biochemical evolution. North-Holland, Amsterdam, pp 89–94Google Scholar
  34. Pace NR (2001) The universal nature of biochemistry. Proc Natl Acad Sci U S A 98:805–808PubMedCentralPubMedCrossRefGoogle Scholar
  35. Pace CN, Scholtz JM (1998) A helix propentisty scale based on experimental studies of peptides and proteins. Biophys J 75:422–427PubMedCentralPubMedCrossRefGoogle Scholar
  36. Padmanabhan S, Baldwin RL (1994) Test for helix-stabilizing interactions between various nonpolar side chains in alanine-based peptides. Protein Sci 3:1992–1997PubMedCentralPubMedCrossRefGoogle Scholar
  37. Parker ET, Cleaves HJ, Dworkin JP et al (2011a) Primordial synthesis of amines and amino acids in a 1958 H2S-rich spark discharge experiment. Proc Natl Acad Sci U S A 108:5526–5531PubMedCentralPubMedCrossRefGoogle Scholar
  38. Parker ET, Cleaves HJ, Callahan MP et al (2011b) Prebiotic synthesis of methionine and other sulfur-containing organic compounds on the primitive Earth: a contemporary reassessment based on an unpublished 1958 Stanley Miller experiment. Orig Life Evol Biosph 41:201–212PubMedCrossRefGoogle Scholar
  39. Philip GK, Freeland SJ (2011) Did evolution select a nonrandom “alphabet” of amino acids? Astrobiology 11:235–240PubMedCrossRefGoogle Scholar
  40. Rajabi M, Ericksen B, Wu X, de Leeuw E, Zhao L, Pazgier M, Lu W (2012) Functional determinants of human enteric a-defensin HD5: crucial role for hydrophobicity at dimer interface. J Biol Chem 287:21615–21627PubMedCentralPubMedCrossRefGoogle Scholar
  41. Ribas De Pouplana L, Schimmel P (2004) Aminoacyl-tRNA synthetases as clues to the establishment of the genetic code. In: Ribas De Pouplana L (ed) The genetic code and the origin of life. Springer US, Georgetown, pp 119–133CrossRefGoogle Scholar
  42. Richmond MH (1962) The effect of amino acid analogues on growth and protein synthesis in microorganisms. Bacteriol Rev 26:398–420PubMedCentralPubMedGoogle Scholar
  43. Ring D, Wolman Y, Friedmann N, Miller SL (1972) Prebiotic synthesis of hydrophobic and protein amino acids. Proc Natl Acad Sci USA 69:765–768Google Scholar
  44. Shen C, Yang L, Miller SL, Oró J (1990) Prebiotic synthesis of histidine. J Mol Evol 31:167–174PubMedCrossRefGoogle Scholar
  45. Soini J, Falschlehner C, Liedert C et al (2008) Norvaline is accumulated after a down-shift of oxygen in Escherichia coli W3110. Microb Cell Factories 7:30CrossRefGoogle Scholar
  46. Tawfik DS (2013) Messy biology and the origins of evolutionary innovations. Nat Chem Biol 6:692–696Google Scholar
  47. Tawfik DS, Khersonsky O (2010) Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem 79:471–505PubMedCrossRefGoogle Scholar
  48. Weber A, Miller S (1981) Reasons for the occurrence of the twenty coded protein amino acids. J Mol Evol 17:273–284PubMedCrossRefGoogle Scholar
  49. White HB III (1976) Coenzymes as fossils of an earlier metabolic state. J Mol Evol 7:101–104PubMedCrossRefGoogle Scholar
  50. Woese CR (1965) On the evolution of the genetic code. Proc Natl Acad Sci U S A 54:1546–1552PubMedCentralPubMedCrossRefGoogle Scholar
  51. Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271PubMedCentralPubMedGoogle Scholar
  52. Wolschner C, Giese A, Kretzschmar HA et al (2009) Design of anti- and pro-aggregation variants to assess the effects of methionine oxidation in human prion protein. Proc Natl Acad Sci U S A 106:7756–7761PubMedCentralPubMedCrossRefGoogle Scholar
  53. Yadavalli SS, Ibba M (2012) Quality control in aminoacyl-tRNA synthesis its role in translational fidelity. Adv Protein Chem Struct Biol 86:1–4PubMedCrossRefGoogle Scholar
  54. Young DD, Young TS, Jahnz M, Ahmad I, Spraggon G, Schultz PG (2011) An evolved aminoacyl-tRNA synthetase with atypical polysubstrate specificity. Biochemistry 50:1894–1900PubMedCentralPubMedCrossRefGoogle Scholar
  55. Zhu B, Zhao M-W, Eriani G, Wang E-D (2007) A present-day aminoacyl-tRNA synthetase with ancestral editing properties. RNA 13:15–21PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Claudia Alvarez-Carreño
    • 1
  • Arturo Becerra
    • 1
  • Antonio Lazcano
    • 1
  1. 1.Facultad de CienciasUniversidad Nacional Autonoma de MexicoMexico D.FMexico

Personalised recommendations