Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-06-21T22:40:18.115Z Has data issue: false hasContentIssue false
  • English
  • Français

Reversible transformation between α-oxo acids and α-amino acids on ZnS particles: a photochemical model for tuning the prebiotic redox homoeostasis

Published online by Cambridge University Press:  29 October 2012

Wei Wang ,
Xiaoyang Liu ,
Yanqiang Yang  and
Wenhui Su
Wei Wang*
Affiliation:
CCMST, Academy of Fundamental and Interdisciplinary Sciences, Harbin Institute of Technology, Harbin 150080, China
Xiaoyang Liu
Affiliation:
State Key Lab of Inorganic Synthesis and Preparative Chemistry, College of Chemistry, Jilin University, Changchun 130012, China
Yanqiang Yang
Affiliation:
CCMST, Academy of Fundamental and Interdisciplinary Sciences, Harbin Institute of Technology, Harbin 150080, China
Wenhui Su
Affiliation:
CCMST, Academy of Fundamental and Interdisciplinary Sciences, Harbin Institute of Technology, Harbin 150080, China
*
e-mail: wwang_ol@hit.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

How prebiotic metabolic pathways could have formed is an essential question for the origins of life on early Earth. From the abiogenetic point of view, the emergence of primordial metabolism may be postulated as a continuum from Earth's geochemical processes to chemoautotrophic biochemical procedures on mineral surfaces. In the present study, we examined in detail the reversible amination of α-ketoglutarate on UV-irradiated ZnS particles under variable reaction conditions such as pH, temperature, hole scavenger species and concentrations, and different amino acids. It was observed that the reductive amination of α-ketoglutarate and the oxidative amination of glutamate were both effectively performed on ZnS surfaces in the presence and absence of a hole scavenger, respectively. Accordingly, a photocatalytic mechanism was proposed. The reversible photochemical reaction was more efficient under basic conditions but independent of temperature in the range of 30–60 °C. SO32− was more effective than S2− as the hole scavenger. Finally, we extended the glutamate dehydrogenase-like chemistry to a set of other α-amino acids and their corresponding α-oxo acids and found that hydrophobic amino acid side chains were more conducive to the reversible redox reactions. Since the experimental conditions are believed to have been prevalent in shallow water hydrothermal vent systems of early Earth, the results of this work not only suggest that the ZnS-assisted photochemical reaction can regulate the redox equilibrium between α-amino acids and α-oxo acids, but also provide a model of how prebiotic metabolic homoeostasis could have been developed and regulated. These findings can advance our understanding of the establishment of archaic non-enzymatic metabolic systems and the origins of autotrophy.

Keywords

amino acidα-oxo acidredox homoeostasisprebiotic metabolismphotocatalysiszinc sulphide
Type
Research Article
Information
International Journal of Astrobiology , Volume 12 , Issue 1 , January 2013 , pp. 69 - 77
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amend, J.P. & Shock, E.L. (1998). Energetics of amino acid synthesis in hydrothermal ecosystems. Science 281, 1659–1662.Google Scholar
Beinert, H., Holm, R.H. & Münck, E. (1997). Iron–sulfur clusters: nature's modular, multipurpose structures. Science 277, 653–659.CrossRefGoogle ScholarPubMed
Bonifačić, M., Štefanić, I., Hug, G.L., Armstrong, D.A. & Asmus, K. (1998). Glycine decarboxylation: the free radical mechanism. J. Am. Chem. Soc. 120, 9930–9940.CrossRefGoogle Scholar
Buxton, G.V., Greenstock, C.L., Helman, W.P. & Ross, A.B. (1988). Critical review of rate constants for reactions of hydrated electrons, hydrogen atoms and hydroxyl radicals (·OH/·O-) in aqueous solution. J. Phys. Chem. Ref. Data 17, 513–886.CrossRefGoogle Scholar
Chen, X., Shen, S., Guo, L. & Mao, S.S. (2010). Semiconductor-based photocatalytic hydrogen generation. Chem. Rev. 110, 6503–6570.CrossRefGoogle ScholarPubMed
Corliss, J.B.et al. (1979). Submarine thermal springs on the Galápagos Rift. Science 203, 1073–1083.Google Scholar
Dupont, C.L., Butcher, A., Valas, R.E., Bourne, P.E. & Caetano-Anollés, G. (2010). History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc. Natl. Acad. Sci. U.S.A. 107, 10567–10572.Google Scholar
Easton, C.J. (1997). Free-radical reactions in the synthesis of α-amino acids and derivatives. Chem. Rev. 97, 53–82.CrossRefGoogle ScholarPubMed
Edmond, J.M., Campbell, A.C., Palmer, M.R., Klinkhammer, G.P., German, C.R., Edmonds, H.N., Elderfield, H., Thompson, G. & Rona, P. (1995). Time series studies of vent fluids from the TAG and MARK sites (1986, 1990) Mid-Atlantic Ridge: a new solution chemistry model and a mechanism for Cu/Zn zonation in massive sulphide orebodies. Geol. Soc. Spec. Publ. 87, 77–86.Google Scholar
Eggins, B.R., Robertson, P.K.J., Stewart, J.H. & Woods, E. (1993). Photoreduction of carbon dioxide on zinc sulfide to give four-carbon and two-carbon acids. Chem. Commun. 349–350.Google Scholar
Guzman, M.I. & Martin, S.T. (2008). Oxaloacetate-to-malate conversion by mineral photoelectrochemistry: implications for the viability of the reductive tricarboxylic acid cycle in prebiotic chemistry. Int. J. Astrobiol. 7, 271–278.Google Scholar
Guzman, M.I. & Martin, S.T. (2009). Prebiotic metabolism: production by mineral photoelectrochemistry of α-ketocarboxylic acids in the reductive tricarboxylic acid cycle. Astrobiology 9, 833–842.Google Scholar
Guzman, M.I. & Martin, S.T. (2010). Photo-production of lactate from glyoxylate: how minerals can facilitate energy storage in a prebiotic world. Chem. Commun. 46, 2265–2267.CrossRefGoogle Scholar
Hartogh, P. et al. (2011). Ocean-like water in the Jupiter-family comet 103P/Hartley 2. Nature 478, 218–220.CrossRefGoogle ScholarPubMed
Hazen, R.M. (2001). Life's rocky start. Sci. Am. 284, 76–85.Google Scholar
Henrichs, S.M. & Sugai, S.F. (1993). Adsorption of amino acids and glucose by sediments of Resurrection Bay, Alaska, USA: functional group effects. Geochim. Cosmochim. Acta 57, 823–835.Google Scholar
Huber, C. & Wächtershäuser, G. (1997). Activated acetic acid by carbon fixation on (Fe,Ni)S under primordial conditions. Science 276, 245–247.Google Scholar
Huber, C., Eisenreich, W., Hecht, S. & Wächtershäuser, G. (2003). A possible primordial peptide cycle. Science 301, 938–940.CrossRefGoogle ScholarPubMed
Berg, J.M., Tymoczko, J.L. & Stryer, L. (2002). Biochemistry. WH Freeman and Company, New York.Google Scholar
Kump, L.R. (2008). The rise of atmospheric oxygen. Nature 451, 277–278.Google Scholar
Li, J. & Pan, Y. (2012). Environmental factors affect magnetite magnetosome synthesis in Magnetospirillum magneticum AMB-1: implications for biologically controlled mineralization. Geomicrobiol. J. 29, 362–373.Google Scholar
Loh, T.P., Wei, L.L. & Feng, L.C. (1999). Direct aldol reactions of glyoxylic acid monohydrate with ketones. Synlett 10, 1059–1060.Google Scholar
Martin, W., Baross, J., Kelley, D. & Russell, M.J. (2008). Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805–814.Google Scholar
Morowitz, H. & Smith, E. (2007). Energy flow and the organization of life. Complexity 13, 51–59.Google Scholar
Mulkidjanian, A.Y. (2009). On the origin of life in the Zinc world: 1. Photosynthesizing, porous edifices built of hydrothermally precipitated zinc sulfide as cradles of life on Earth. Biol. Direct. 4, 26.Google Scholar
Mulkidjanian, A.Y. & Galperin, M.Y. (2009). On the origin of life in the Zinc world: 2. Validation of the hypothesis on the photosynthesizing zinc sulfide edifices as cradles of life on Earth. Biol. Direct. 4, 27.Google Scholar
Orgel, L.E. (2000). Self-organizing biochemical cycles. Proc. Natl. Acad. Sci. U.S.A. 97, 12503–12507.Google Scholar
Owen, O.E., Kalhan, S.C. & Hanson, R.W. (2002). The key role of anaplerosis and cataplerosis for citric acid cycle function. J. Biol. Chem. 277, 30409–30412.Google Scholar
Ranjit, K.T., Krishnamoorthy, R. & Viswanathan, B. (1994). Photocatalytic reduction of nitrite and nitrate on ZnS. J. Photochem. Photobiol. A: Chem. 81, 55–58.CrossRefGoogle Scholar
Reber, J. & Meier, K. (1984). Photochemical production of hydrogen with zinc sulfide suspensions. J. Phys. Chem. 88, 5903–5913.Google Scholar
Russell, M.J. (2007). The alkaline solution to the emergence of life: energy, entropy and early evolution. Acta Biotheor. 55, 133–179.CrossRefGoogle Scholar
Russell, M.J. & Hall, A.J. (1997). The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J. Geol. Soc. 154, 377–402.Google Scholar
Russell, M.J. & Martin, W. (2004). The rocky roots of the acetyl-CoA pathway. Trends Biochem. Sci. 29, 358–363.Google Scholar
Russell, M.J., Daniel, R.M., Hall, A.J. & Sherringham, J.A. (1994). A hydrothermally precipitated catalytic iron sulphide membrane as a first step toward life. J. Mol. Evol. 39, 231–243.Google Scholar
Rustgi, S., Joshi, A., Moss, H. & Riesz, P. (1977). ESR of spin-trapped radicals in aqueous solutions of amino acids. Reactions of the hydroxyl radical. Int. J. Radiat. Biol. 31, 415–440.Google Scholar
Saladino, R., Crestini, C., Pino, S., Costanzo, G. & Di Mauro, E. (2012). Formamide and the origin of life. Phys. Life Rev. 9, 84–104.Google Scholar
Smith, E. & Morowitz, H.J. (2004). Universality in intermediary metabolism. Proc. Natl. Acad. Sci. U.S.A. 101, 13168–13173.Google Scholar
Tarasov, V.G., Gebruk, A.V., Mironov, A.N. & Moskalev, L.I. (2005). Deep-sea and shallow-water hydrothermal vent communities: two different phenomena? Chem. Geol. 224, 5–39.Google Scholar
Tivey, M.K., Stakes, D.S., Cook, T.L., Hannington, M.D. & Petersen, S. (1999). A model for growth of steep-sided vent structures on the endeavour SEGMENT of the Juan de Fuca Ridge: results of a petrologic and geochemical study. J. Geophys. Res. 104, 22859–22883.Google Scholar
Wächtershäuser, G. (1988). Before enzymes and templates: theory of surface metabolism. Microbiol. Rev. 52, 452–484.Google Scholar
Wächtershäuser, G. (2007). On the chemistry and evolution of the pioneer organism. Chem. Biodivers. 4, 584–602.Google Scholar
Wang, W., Li, Q., Yang, B., Liu, X., Yang, Y. & Su, W. (2012a). Enhanced photocatalytic performance of ZnS for reversible amination of α-oxo acids by hydrothermal treatment. Orig. Life Evol. Biosph. 42, 263–273.Google Scholar
Wang, W., Li, Q., Yang, B., Liu, X., Yang, Y. & Su, W. (2012b). Photocatalytic reversible amination of α-keto acids on a ZnS surface: implications for the prebiotic metabolism. Chem. Commun. 48, 2146–2148.CrossRefGoogle ScholarPubMed
Wang, W., Qu, Y., Yang, B., Liu, X. & Su, W. (2012c). Lactate oxidation in pyrite suspension: a Fenton-like process in situ generating H2O2. Chemosphere 86, 376–382.CrossRefGoogle ScholarPubMed
Wang, W., Yang, B., Qu, Y., Liu, X. & Su, W. (2011). FeS/S/FeS2 redox system and its oxidoreductase-like chemistry in the iron–sulfur world. Astrobiology 11, 471–476.Google Scholar
Warren, W.A. (1971). Carbanion generation and aldol condensation between glyoxylate and glycine of glycinamide. Arch. Biochem. Biophys. 143, 212–217.Google Scholar
Xu, Y. & Schoonen, M.A.A. (2000). The absolute energy positions of conduction and valence bands of selected semiconducting minerals. Am. Mineral. 85, 543–556.Google Scholar
Zhang, X.V. & Martin, S.T. (2006). Driving parts of Krebs cycle in reverse through mineral photochemistry. J. Am. Chem. Soc. 128, 16032–16033.Google Scholar
Supplementary material: File

Wang Supplementary Material

Appendix

Download Wang Supplementary Material(File)
File 33.5 KB