Synthesis 2021; 53(16): 2798-2808
DOI: 10.1055/a-1472-7914
short review

Sulfur Amino Acids: From Prebiotic Chemistry to Biology and Vice Versa

Sparta Youssef-Saliba
,
The research was funded by Agence Nationale de la Recherche in the framework of the Investissements d’Avenir program (ANR-15-IDEX-02), through the funding of the ‘Origin of Life’ project of the Université Grenoble-Alpes, Labex ARCANE, and CBH-EUR-GS (ANR-17-EURE-0003).


Abstract

Two sulfur-containing amino acids are included in the list of the 20 classical protein amino acids. A methionine residue is introduced at the start of the synthesis of all current proteins. Cysteine, thanks to its thiol function, plays an essential role in a very large number of catalytic sites. Here we present what is known about the prebiotic synthesis of these two amino acids and homocysteine, and we discuss their introduction into primitive peptides and more elaborate proteins.

1 Introduction

2 Sulfur Sources

3 Prebiotic Synthesis of Cysteine

4 Prebiotic Synthesis of Methionine

5 Homocysteine and Its Thiolactone

6 Methionine and Cystine in Proteins

7 Prebiotic Scenarios Using Sulfur Amino Acids

8 Introduction of Cys and Met in the Genetic Code

9 Conclusion



Publication History

Received: 11 February 2021

Accepted after revision: 01 April 2021

Accepted Manuscript online:
01 April 2021

Article published online:
22 April 2021

© 2021. Thieme. All rights reserved

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Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References


    • Reviews, inter alia:
    • 1a Eschenmoser A. Tetrahedron 2007; 63: 12821
    • 1b Danger G, Plasson R, Pascal R. Chem. Soc. Rev. 2012; 41: 5416
    • 1c Saladino R, Botta G, Pino S, Costanzo G, Di Mauro E. Chem. Soc. Rev. 2012; 41: 5526
    • 1d Ruiz-Mirazo K, Briones C, de la Escosura A. Chem. Rev. 2014; 114: 285
    • 1e Sutherland JD. Angew. Chem. Int. Ed. 2016; 55: 104
    • 1f Kitadai N, Maruyama S. Geosci. Front. 2018; 9: 1117
    • 1g Yadav M, Kumar R, Krishnamurthy R. Chem. Rev. 2020; 120: 4766
    • 1h Muchowska KB, Varma SJ, Moran J. Chem. Rev. 2020; 120: 7708
    • 1i Bizzarri BM, Saladino R, Delfino I, García-Ruiz JM, Di Mauro E. Int. J. Mol. Sci. 2021; 22: 917

    • Recent work:
    • 1j Botta L, Saladino R, Bizzarri BM, Cobucci-Ponzano B, Iacono R, Avino R, Caliro S, Carandente A, Lorenzini F, Tortora A, Di Mauro E, Moracci M. Adv. Space Res. 2018; 62: 2372
    • 1k Bizzarri BM, Botta L, Pérez-Valverde MI, Saladino R, Di Mauro E, García-Ruiz JM. Chem. Eur. J. 2018; 24: 8126
  • 2 Kozlowski LP. Nucleic Acids Res. 2017; 45: 1112
  • 3 Bartlett GJ, Porter CT, Borkakoti N, Thornton JM. J. Mol. Biol. 2002; 324: 105
  • 4 Oppenheimer C, Scaillet B, Martin RS. Rev. Mineral. Geochem. 2011; 73: 363
  • 5 Lee S, Kang N, Park M, Hwang JY, Yun SH, Jeong HY. Geosci. J. 2018; 22: 183
  • 6 Aiuppa A, Federico C, Giudice G, Gurrieri S, Valenza M. Geophys. Res. Lett. 2006; 33: 21315
  • 7 Ohba T, Hirabayashi J, Yoshida M. J. Volcanol. Geotherm. Res. 1994; 60: 263
  • 8 Saturno J, Ditas F, Penning de Vries M, Holanda BA, Pöhlker ML, Carbone S, Walter D, Bobrowski N, Brito J, Chi X, Gutmann A, Hrabe de Angelis I, Machado LA. T, Moran-Zuloaga D, Rüdiger J, Schneider J, Schulz C, Wang Q, Wendisch M, Artaxo P, Wagner T, Pöschl U, Andreae MO, Pöhlker C. Atmos. Chem. Phys. 2018; 18: 10391
  • 9 Reeves EP, McDermott JM, Seewald JS. Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 5474
  • 10 Sydow L, Bennett PC, Nordstrom DK. Procedia Earth Planet. Sci. 2017; 17: 504
  • 12 Orgel LE. Origins Life Evol. Biospheres 1998; 28: 227
  • 13 Barton LL, Fauque GD. Adv. Appl. Microbiol. 2009; 68: 41
  • 14 Grein F, Ramos AR, Venceslau SS, Pereira IA. C. Biochim. Biophys. Acta 2013; 1827: 145
  • 15 Santos AA, Venceslau SS, Grein F, Leavitt WD, Dahl C, Johnston DT, Pereira IA. C. Science 2015; 350: 1541
  • 16 Ravot G, Ollivier B, Magot M, Patel BK. C, Crolet JL, Fardeau ML, Garcia JL. Appl. Environ. Microbiol. 1995; 61: 2053
  • 17 Melideo SL, Jackson MR, Jorns MS. Biochemistry 2014; 53: 4739
  • 18 Boulegue J. Dev. Econ. Geol. 1981; 15: 21
  • 19 Cypionka H, Smock AM, Böttcher ME. FEMS Microbiol. Lett. 1998; 166: 181
    • 20a Mißbach H, Duda J.-P, van den Kerkhof AM, Lüders V, Pack A, Reitner J, Thiel V. Nat. Commun. 2021; 12: 1101
    • 20b Havig JR, Hamilton TL, Bachan A, Kump LR. Earth-Sci. Rev. 2017; 174: 1
  • 21 Fakhraee M, Katsev S. Nat. Commun. 2019; 10: 4556
  • 22 Armstrong RW, Arkayin B, Haddad G. Nature 1971; 232: 577
  • 23 Hennet RJ. C, Holm NG, Engel MH. Naturwissenschaften 1992; 79: 361
    • 24a Parker ET, Cleaves HJ, Dworkin JP, Glavin DP, Callahan M, Aubrey M, Lazcano A, Bada JL. Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 5526
    • 24b About the synthesis of other amino acids under similar conditions see: Ring D, Wolman Y, Friedmann N, Miller SL. Proc. Natl. Acad. Sci. U. S. A. 1972; 69: 765
  • 25 Shalayel I, Youssef-Saliba S, Vazart F, Ceccarelli C, Bridoux M, Vallée Y. Eur. J. Org. Chem. 2020; 2020: 3019
  • 26 Vazart F, Balucani N, Skouteris D, Ceccarelli C, Shalayel I, Vallee Y. Mem. Soc. Astron. Ital. 2019; 90: 467
  • 27 Youssef-Saliba S, Vallée Y. Curr. Org. Chem. 2020; 24: 774
  • 28 Foden CS, Islam S, Fernández-García C, Maugeri L, Sheppard TD, Powner MW. Science 2020; 370: 865
  • 29 Borup B, Ferry JG. FEMS Microbiol. Lett. 2000; 189: 205
  • 30 Nakatani T, Ohtsu I, Nonaka G, Wiriyathanawudhiwong N, Morigasaki S, Takagi H. Microb. Cell Fact. 2012; 11: 62
  • 31 Griffith OW. Methods Enzymol. 1987; 143: 366
  • 32 Kitabatake M, So MW, Tumbula DL, Soll S. J. Bacteriol. 2000; 182: 143
  • 33 Van Trump JE, Miller SL. Science 1972; 178: 859
  • 34 Parker ET, Cleaves HJ, Callahan MP, Dworkin JP, Glavin DP, Lazcano A, Bada JL. Origins Life Evol. Biospheres 2011; 41: 201
  • 35 Zahnle KJ. J. Geophys. Res. 1986; 91: 2819
  • 36 Smith AE, Silver JJ, Steinman G. Science 1968; 159: 1108
  • 37 Hatanaka H, Egami F. Bull. Chem. Soc. Jpn. 1977; 50: 1147
  • 38 Ferla MP, Patrick WM. Microbiology 2014; 160: 1571
  • 39 Shalayel I, Vallée Y. Life 2019; 9: 40 DOI: 10.3390/life9020040.
  • 40 de Duve C. Origins Life Evol. Biospheres 2003; 33: 559
  • 41 Jakubowski H. Life 2017; 7: 6
  • 42 Jakubowski H. EMBO J. 1991; 3: 598
  • 43 Perla-Kajan J, Twardowski T, Jakubowski H. Amino Acids 2007; 32: 561
  • 44 Boldyrev AA. Biochemistry (Moscow) 2009; 74: 589
  • 45 Demongeot J, Seligmann H. BioEssays 2020; 42: 1900201
  • 46 Blattner FR, Plunkett GIII, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. Science 1997; 277: 1453
  • 47 Sacerdot C, Fayat G, Dessen P, Springer M, Plumbridge JA, Gninberg-Manago M, Blanquet S. EMBO J. 1982; 1: 311
  • 48 Missiakas D, Georgopoulos C, Raina S. J. Bacteriol. 1993; 175: 2613
  • 49 Belinky F, Rogozin IB, Koonin EV. Sci. Rep. 2017; 7: 12422
  • 50 Vallée Y, Milet A, Rao KV. R. Phosphorus, Sulfur Silicon Relat. Elem. 2016; 191: 329
  • 51 Raghavendra Rao KV, Vallée Y. Tetrahedron 2016; 72: 4442
  • 52 Raghavendra Rao KV, Caiveau N, David R, Shalayel I, Milet A, Vallée Y. Eur. J. Org. Chem. 2015; 2015: 6125
  • 53 Rubino JT, Chenkin MP, Keller M, Riggs-Gelascob P, Franz KJ. Metallomics 2011; 3: 61
  • 54 Deepak RN. V. K, Chandrakar B, Sankararamakrishnan R. Biophys. Chem. 2017; 224: 32
  • 55 Stadtman ER, Remmen HV, Richardson A, Wehr NB, Levine RL. Biochim. Biophys. Acta 2005; 1703: 135
  • 56 Valley CC, Cembran A, Perlmutter JD, Lewis AK, Labello NP, Gao J, Sachs JN. J. Biol. Chem. 2012; 287: 34979
  • 57 Cirino PC, Tang Y, Takahashi K, Tirrell DA, Arnold FH. Biotechnol. Bioeng. 2003; 83: 729
  • 58 Alvarez-Carreño C, Becerra A, Lazcano A. Origins Life Evol. Biospheres 2013; 43: 363
  • 59 Starck SR, Jiang V, Pavon-Eternod M, Prasad S, McCarthy B, Pan T, Shastri N. Science 2012; 336: 1719
  • 60 Anfinsen CB. Science 1973; 181: 4096
  • 61 Qin M, Wang W, Thirumalai D. Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 11241
  • 62 Hatahet F, Ruddock LW. Antioxid. Redox Signaling 2009; 11: 2807
  • 63 Rajpal G, Arvan P. Disulfide Bond Formation . In Handbook of Biologically Active Peptides, 2nd ed. Kastin AJ. Academic Press; San Diego: 2013: 1721
  • 64 Jorda J, Yeates TO. Archaea 2011; 2011: 409156
  • 65 Buchanan BB, Holmgren A, Jacquot J.-P, Scheibe R. Biochim. Biophys. Acta 2012; 1820: 1822
  • 66 Claiborne A, Yeh JI, Mallett TC, Luba J, Crane EJ, Charrier V, Parsonage D. Biochemistry 1999; 38: 15407
  • 67 Wood ZA, Schröder E, Harris JR, Poole LB. Trends Biochem. Sci. 2003; 28: 32
    • 68a Wei Y, Funk MA, Rosado LA, Baek J, Drennan CL, Stubbe J. Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 3756
    • 68b Kolberg M, Strand KR, Graff P, Andersson KK. Biochem. Biophys. Acta 2004; 1699: 1
    • 68c Lundin D, Berggren G, Logan DT, Sjöberg B.-M. Life 2015; 5: 604 DOI: 10.3390/life5010604.
  • 69 Torrents E, Aloy P, Gibert I, Rodriguez-Trelles F. J. Mol. Evol. 2002; 55: 138
  • 70 Hardy LW, Finer-Moore JS, Montfort WR, Jones MO, Santi DV, Stroud RM. Science 1987; 235: 448
  • 71 Johnson DC, Dean DR, Smith AD, Johnson MK. Annu. Rev. Biochem. 2005; 74: 247
  • 72 Wu Y, Brosh RM. Jr. Nucleic Acids Res. 2012; 40: 4247
  • 73 Brown EN, Friemann R, Karlsson A, Parales JV, Couture MM.-J, Eltis LD, Ramaswamy S. J. Biol. Inorg. Chem. 2008; 13: 1301
  • 74 Bonfio C, Valer L, Scintilla S, Shah S, Evans DJ, Jin L, Szostak JW, Sasselov DD, Sutherland JD, Mansy SS. Nat. Chem. 2017; 9: 1229
  • 75 Kim JD, Pike DH, Tyryshkin AM, Swapna GV. T, Raanan H, Montelione GT, Nanda V, Falkowski PG. J. Am. Chem. Soc. 2018; 140: 11210
  • 76 Fleminger G, Yaron T, Eisenstein M, Bar-Nun A. Origins Life Evol. Biospheres 2005; 35: 369
  • 78 Fuss JO, Tsai C, Ishida JP, Tainer JA. Biochim. Biophys. Acta 2015; 1853: 1253
  • 79 Baranovskiy AG, Siebler HM, Pavlov YI, Tahirov TH. Methods Enzymol. 2018; 599: 1
  • 80 Weiner BE, Huang H, Dattilo BM, Nilges MJ, Fanning E, Chazin WJ. J. Biol. Chem. 2007; 282: 33444
  • 81 Kimura S, Suzuki T. Biochim. Biophys. Acta 2015; 1853: 1272
  • 82 Brown RS. Curr. Opin. Struct. Biol. 2005; 15: 94
  • 83 Laity JH, Lee BM, Wright PE. Curr. Opin. Struct. Biol. 2001; 11: 39
  • 84 Klug A. Annu. Rev. Biochem. 2010; 79: 213
  • 85 Nikolaev I, Cochet M.-F, Lenouvel F, Felenbok B. Mol. Microbiol. 1999; 31: 1115
  • 86 Taylor SR. Geochim. Cosmochim. Acta 1964; 28: 1273
  • 87 Nagel C, Machulla A, Zahn S, Soppa J. Genes 2019; 10: 361 org/10.3390/genes10050361
  • 88 Petrov AS, Gulen B, Norris AM, Kovacs NA, Bernier CR, Lanier KA, Fox GE, Harvey SC, Wartell RM, Hud NV, Williams LD. Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 15396
  • 89 Ramakrishnan V, White SW. Trends Biochem. Sci. 1998; 23: 208
  • 90 Lupas AN, Alva V. J. Struct. Biol. 2017; 198: 74
  • 91 Chan Y, Suzuki K, Olvera J, Wool IG. Nucleic Acids Res. 1993; 21: 649
  • 92 Wu B, Lukin J, Yee A, Lemak A, Semesi A, Ramelot TA, Kennedy MA, Arrowsmith CH. Protein Sci. 2008; 17: 589
  • 93 Bergmann U, Wittmann-Liebold B. Biochim. Biophys. Acta 1993; 1173: 195
  • 94 Jeganathan A, Razi A, Thurlow B, Ortega J. RNA 2015; 21: 1203
  • 95 Chen K, Roberts E, Luthey-Schulten Z. BMC Evol. Biol. 2009; 9: 179
  • 96 Dresios J, Chan Y, Wool IG. J. Mol. Biol. 2002; 316: 475
  • 97 Wool IG, Chan Y, Glück A. Biochem. Cell Biol. 1995; 73: 933
  • 98 Wu M, Filley SJ, Xiong J, Lee JJ, Hill KA. W. Biochemistry 1994; 33: 12260
  • 99 Banerjee R, Dubois DY, Gauthier J, Lin S, Roy S, Lapointe J. Eur. J. Biochem. 2004; 271: 724
  • 100 Landro JA, Schimmel P. Proc. Natl. Acad. Sci. U. S. A. 1993; 90: 2261
  • 101 Newberry KJ, Hou Y, Perona JJ. EMBO J. 2002; 21: 2778
  • 102 Shimberg GD, Michalek JL, Oluyadi AA, Rodrigues AV, Zucconi BE, Neu HM, Ghosh S, Sureschandra K, Wilson GM, Stemmler TL, Michel SL. J. Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 4700
  • 103 Festa RA, Thiele DJ. Curr. Biol. 2011; 21: 877
  • 104 Holm RH, Kennepohl P, Solomon EI. Chem. Rev. 1996; 96: 2239
    • 105a Russell JR, Martin W. Trends Biochem. Sci. 2004; 29: 358
    • 105b Can M, Armstrong FA, Ragsdale SW. Chem. Rev. 2014; 114: 4149
    • 105c For enzymes (nitrate reductases, formate dehydrogenases) containing both iron and molybdenum, see: Rothery RA, Workun GJ, Weiner JH. Biochem. Biophys. Acta 2008; 1778: 1897
  • 106 Dodson G, Wlodawer A. Trends Biochem. Sci. 1998; 23: 347
  • 107 Strieker M, Tanović A, Marahiel MA. Curr. Opin. Struct. Biol. 2010; 20: 234
  • 108 Roger R, Neilson DG. Chem. Rev. 1961; 61: 179
    • 109a Vallée Y, Shalayel I, Ly KD, Raghavendra Rao KV, De Paëpe G, Märker K, Millet A. Int. J. Dev. Biol. 2017; 61: 471
    • 109b Shalayel I, Coulibaly S, Ly KD, Milet A, Vallée Y. Life 2018; 8: 47; 103390/life8040047
  • 110 Canavelli P, Islam S, Powner MW. Nature 2019; 571: 546

    • Possibly prebiotic syntheses of thioesters:
    • 111a Weber AL. J. Mol. Evol. 1984; 20: 157
    • 111b Huber C, Wächtershäuser G. Science 1997; 281: 670
    • 111c Leqraa N, Nicolet Y, Milet A, Vallée Y. Sci. Rep. 2020; 10: 14488
    • 111d Chevallot-Beroux E, Gorges J, Moran J. ChemRxiv 2019; preprint DOI: 10.26434/chemrxiv.8832425.v1.
  • 112 Trifonov EN. J. Biomol. Struct. Dyn. 2004; 22: 1
  • 113 Yuan J, Palioura S, Salazar JC, Su D, O’Donoghue P, Hohn MJ, Cardoso AM, Whitman WB, Söll D. Proc. Natl. Acad. Sci. U. S. A. 2006; 103: 18923
  • 114 Novozhilov AS, Koonin EV. Biol. Direct 2009; 4: 44
  • 115 Baumann U, Oro J. BioSystems 1993; 29: 133
  • 116 Bonfio C. Dalton Trans. 2021; 50: 801
  • 117 Bourgis F, Roje S, Nuccio ML, Fischer DB, Tarczynski MC, Li C, Herschbach C, Rennenberg H, Pimenta MJ, Shen T.-L, Gage DA, Hanson AD. Plant Cell 1999; 11: 1485
  • 118 Perna AF, Ingrosso D, Lombardi C, Acanfora F, Satta E, Cesare CM, Violetti E, Romano MM, De Santo NG. Kidney Int. 2003; 63: S137
  • 119 Jakubowski H. Physiol. Rev. 2019; 99: 555