The Conservation of Homochirality and Prebiotic Synthesis of Amino Acids
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1 The Conservation of Homochirality and Prebiotic Synthesis of Amino Acids Harold J. Morowitz SFI WORKING PAPER: SFI Working Papers contain accounts of scientific work of the author(s) and do not necessarily represent the views of the Santa Fe Institute. We accept papers intended for publication in peer-reviewed journals or proceedings volumes, but not papers that have already appeared in print. Except for papers by our external faculty, papers must be based on work done at SFI, inspired by an invited visit to or collaboration at SFI, or funded by an SFI grant. NOTICE: This working paper is included by permission of the contributing author(s) as a means to ensure timely distribution of the scholarly and technical work on a non-commercial basis. Copyright and all rights therein are maintained by the author(s). It is understood that all persons copying this information will adhere to the terms and constraints invoked by each author's copyright. These works may be reposted only with the explicit permission of the copyright holder. SANTA FE INSTITUTE
2 The Conservation of Homochirality and the Prebiotic Synthesis of Amino Acids Harold J. Morowitz Krasnow Institute of Advanced Study George Mason University Fairfax, Virginia In autotrophs all synthetic pathways for amino acids except that for glutamic acid involve a transamination reaction with a glutamate donor. It is argued that these reactions conserve chirality so that the homochirality of glutamate generates 18 amino acids of the same stereospecificity. The role of pyridoxal phosphate is explored with respect to biotic and prebiotic transamination. The reason for amino acids and sugars having different stereospecificities is discussed for synthesis of essential compounds involving both an amino acid and a sugar. A generalization of ecological biochemistry is that nitrogen enters into covalent bonding with biochemicals in its most reduced form, ammonia. A series of intermediate oxidations and reductions may precede incorporation, but the nitrogen bonded to carbon is in the form of an amine. In autotrophs the incorporation of ammonia is almost entirely by the following pathways: 1. α-ketoglutarate + NH 3 Glutamate 2. Glutamate + NH 3 Glutamine 3. Aspartate + NH 3 Asparagine 4. Carbonate + NH 3 + Phosphate Carbamoyl phosphate
3 All amino acid synthetic pathways leading to an amine attached to the α carbon of an amino acid are through a glutamate, which is synthesized by Reaction 1 above or a related reaction, Glutamine + α-ketoglutarate 2 Glutamate. All amino acids except glutamate involve in their synthetic pathway a transamination in which glutamate is the donor of the amine group. (See Table I.) The argument then follows that if glutamate is homochiral and if homochirality is conserved in transamination reactions, then all chiral amino acids will have the same chirality as glutamate. What then are the universal characteristics of biological transamination reactions? They all involve an amine donor, an intermediate, and a ketone or keto acid receptor. The universal intermediate is pyridoxal phosphate tightly bound to a protein. In present day biochemistry, the pyridoxal is tightly bound to the ε amine of a lysine of the transaminase enzyme, forming a Schiff base. Transamination then occurs by the Ping-Pong reaction as described in Lehninger Principles of Biochemistry Third Edition 1 as Amniotransferases are classic examples of enzymes catalyzing bimolecular Ping-Pong reactions in which the first substrate reacts, then the product must leave the active site before the second substrate can bind. Thus the incoming amino acid binds to the active site, donates its amino group to pyridoxal phosphate, and departs in the form of an α-keto acid. The incoming α-keto acid then binds, accepts the amino group from pyridoxamine phosphate, and departs in the form of an amino acid. The intermediate pyridoxamine phosphate would not be chiral in solution, but because it is rigidly bound to a surface, the most favorable path for the incoming keto acid is the reverse of 2
4 the departing path of the amino donor. This results in the synthesized amino acid having the same chirality as the donor glutamate. Homochirality is thus conserved, and the steric configuration of glutamate, which is L, is conserved in all the coded amino acids except for the non-chiral glycine. Amino acids must have preceded proteins. If pyrdoxal is involved in primordial amino acid synthesis, it must be synthesized and rigidly attached to a surface in order to conserve chirality. Possible surfaces are crystals, clays, and non-polar phases. Starting with glycoaldehyde and ammonia, S.M. Austin and T.G. Waddell 2 have randomly synthesized a family of pyridine molecules from simple percursors, suggesting the prebiotic presence of molecules capable of Pong-Pong reactions. The presence and role of vitamin B6-type compounds under prebiotic conditions thus becomes an experimental question and one of great importance. Pyridoxal phosphate also catalyzes decarboxyalations, racemizations, and aldol condensations. Because of the Schiff base formations, it is something of a universal catalyst and one that can presumably act without the protein moiety, particularly if it is attached to a surface. One can see an emerging logic of the metabolic chart, which in the first instance is related to the network autocatalytic nature of the reductive citric acid cycle 3, 4 and in the second instance relates to the universality of the transaminating reaction in all pathways to amino acid synthesis. 3
5 Although we do not fully understand the origin of the chart of intermediary metabolism, our present knowledge points to a logic which I believe we will one day understand as we now comprehend structures like the periodic table of the elements. In any case, the universality of L amino acids involves only one choice, not 19. Since pyridoxal phosphate is such a key molecule, we look at the present synthetic pathways to its synthesis. 5 There seem to be two distinct and exclusive pathways with no overlap in enzymes or amino acid sequences. The first, involving the SORI genes, is widely distributed among all the major taxa. The second pathway is distributed among a number of not closely related eubacteria and requires genes designated pdxa and pdxj. No species appears to contain both SORI and the pdxa, pdxj complex. The E. coli pathway 6 is shown in Figure 1. The intermediate 4 Phospho-hydroxy-Lthreonine contains an L chiral center from glutanate and a D chiral center from Erythrose, which ultimately comes from D-glyceraldehyde-3-phosphate, the original chiral sugar, whose D homochirality is universal in the successor sugars. The DL (4 Phosphohydroxy L-threonine) and the D 1-Deoxy-D-xylolose-5-phosphate condense to form the non-chiral Piridoxine 5-phosphate. At this point the D-ness of the sugars and L-ness of the amino acids come together to generate the chirality-conserving molecule Pyridoxine-5-phosphate. This appears to be a critical checkpoint in the master stereochemistry of the metabolic map. It suggests D sugars and L amino acids are not independent, but are linked in a network where sugars and amino acids come together to form nitrogen heterocycles and all manner of prosthetic groups and cofactors. The 4
6 amino acid synthetic pathways reduce 19 choices to one, and the nodes in the metabolic chart, where more complex syntheses involve both sugar and amino acid derivatives, reduce the total choices from two to one. We have not eliminated the possibility of a world of L sugars and D amino acids. A study of metabolic pathways gives insight into some puzzling questions of biogenesis. This report extends several years of investigation begun at a sabbatical at the Santa Fe Institute and involves ongoing discussion with several members of the Santa Fe family. I also want to acknowledge discussions with members of the Astrobiology group at the Carnegie Institute of Washington and the Department of Ecology and Evolutionary Biology at Yale. 5
7 Table I Amino Acid Entry Point of Amino Nitrogen 1. Alanine Pyruvate + Glutamate 2. Arginine α-ketoglutarate + Ammonia 3. Asparagine Oxaloacetate + Glutamate 4. Aspartate Oxaloacetate + Glutamate 5. Cysteine 3 Phosphohydroxypyruvate + Glutamate 6. Glutamate α-ketoglutarate + Ammonia 7. Glutamine Ammonia + Glutamate 8. Glycine 3 Phosphohydroxypyruvate + Glutamate 9. Histidine Imidazol acetalphosphate + Glutamate 10. Isoleucine α-ketomethylvalerate + Glutamate 11. Leucine α-ketoisocaproate + Glutamate 12. Lysine α-ketoadiptate + Glutamate 13. Methionine Oxaloacetate + Glutamate 14. Phenylalanine Phenyl pyruvate+ Glutamate 15. Proline α-ketoglutarate + Ammonia 16. Serine 3 Phosphohydroxypyruvate + Glutamate 17. Threonine Oxaloacetate + Glutamate 18. Tryptophan 3 Phosphohydroxypyruvate + Glutamate 19. Tyrosine 4 Hydroxyphenylpyruvate+ Glutamate 20. Valine α-ketoisovalerate + Glutamate 6
8 Figure 1 D-Erythrose 4-Phospho- 3 Hydroxy- 4 Phospho- 4-phosphate erythronate 4 phospho- hydroxyhydroxy- L-threonine α-ketobutyrate + Glutamate pyridoxine 5 ' -phosphate Pyruvate+D-Glyceraldehyde 1-Deoxy-D -3-phosphate xylulose- 5-phosphate 7
9 References 1. Nelson, D.L., and Cox, M. M., Lehninger Principles of Biochemistry (Worth, 2000), pp [third edition] 2. Austin, S. M., Waddell, T. G., "Prebiotic Synthesis of Vitamin B6-type Compounds," Origins of Life and Evolution of the Biosphere 29, pp (1997). 3. Morowitz, H. J., Kostelnik, J. D., Yang, J., Cody, G. D., "The Origin of Intermediary Metabolism," Proc. Natl. Acad. Sci. U.S.A. 97, (2000). 4. Morowitz, H. J., "A Theory of Biochemical Organization, Metabolic Pathways, and Evolution," Complexity 4, (1999). 5. Ehrenshaft, M., Bilski, P., Li, M. Y., Chignell, C. F., Daub, M. E., "A Highly Conserved Sequence Is a Novel Gene Involved in de novo Vitamin B6 Biosynthesis," Proc. Natl. Acad. Sci. U.S.A. 96, (1999). 6. Yang, Y., Zhao, G., Man, T., Winkler, M. E., " Involvement of the gapa- and epd (gapb)-encoded Dehydrogenases in Pyridoxal 5'-Phosphate Coenzyme Biosynthesis in Escherichia coli K-12," J. Bact. 180, (1998). 8
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