Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-23T07:52:02.924Z Has data issue: false hasContentIssue false

Critical role of spatial information from chiral-asymmetric peptides in the earliest occurrence of life

Published online by Cambridge University Press:  19 January 2016

Hugo I. Cruz-Rosas*
Affiliation:
Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP. 04510, D. F., Mexico Instituto de Física, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP. 04510, D. F., Mexico
Francisco Riquelme
Affiliation:
Paleobiología, Escuela de Estudios Superiores del Jicarero, Universidad Autónoma del Estado de Morelos, Jicarero CP. 62909, Morelos, Mexico
Mariel Maldonado
Affiliation:
Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP. 04510, D.F., Mexico
Germinal Cocho*
Affiliation:
Instituto de Física, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP. 04510, D. F., Mexico

Abstract

The earliest functional living system on Earth should have been able to reproduce an ordered configuration and a self-organization dynamics. It was capable of resisting a random variability in time and space to keep the functionality. Amino acids (AAs) and nucleobases generated from abiotic reactions as seen in laboratory-based experiments have demonstrated that molecular elements for life can be obtained by predictable physicochemical processes. However, a functional, self-organized living system needs complex molecular interactions to endure. In this paper, we address the transference of spatial information on highly enantiopure polymers as a critical condition to support the dynamics in a self-organized biogenic system. Previous scenarios have considered almost exclusively the information encoded in sequences as the suitable source of prebiotic information. But the spatial information transference has been poorly understood thus far. We provide the supporting statements which predict that the ordered configuration in a biogenic system should be significantly influenced by spatial information, instead of being exclusively generated by sequences of polymers. This theoretical approach takes into consideration that the properties of mutation and inheritance did not develop before definition of the structures that allow the management of information. Rather, we postulate that the molecular structures to store and transfer information must exist at first, in order to retain particular functional ‘meaning’, and subsequently, such information can be ‘inherited’ and eventually modified. Thus, the present contribution follows the theory that life was originated from an unstable prebiotic environment that involves the early spatial information transference based on large chiral asymmetry.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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

Arteaga, O., Canillas, A., Crusats, J., El-Hachemi, Z., Jellison, G.E. Jr., Llorca, J. & Ribó, J.M. (2010). Chiral biases in solids by effect of shear gradients: a speculation on the deterministic origin of biological homochirality. Orig. Life Evol. Biosph. 40, 2740.Google Scholar
Berthod, A. (2006). Chiral recognition mechanisms. Anal. Chem. 78(7), 20932099.CrossRefGoogle ScholarPubMed
Bonner, W.A. (1995). Chirality and life. Orig. Life Evol. Biosph. 25, 175190.Google Scholar
Bonner, W.A., Greenberg, J.M. & Rubenstein, E. (1999). The extraterrestrial origin of the homochirality of biomolecules-rebuttal to a critique. Orig. Life Evol. Biosph. 29, 215219.Google Scholar
Brack, A. (1977). β-Structures of alternating polypeptides and their possible role in chemical evolution. Biosystems 9, 99103.Google Scholar
Brack, A. (2007). From interstellar amino acids to prebiotic catalytic peptides: a review. Chem. Biodivers. 4(4), 665679.Google Scholar
Brack, A. & Orgel, L.E. (1975). β-Structures of alternating polypeptides and their possible prebiotic significance. Nature 256, 383387.CrossRefGoogle ScholarPubMed
Carroll, J.D. (2009). A new definition of life. Chirality 21, 354358.CrossRefGoogle ScholarPubMed
Chakrabarti, P. & Janin, J. (2002). Dissecting protein–protein recognition sites. Proteins 47(3), 334343.Google Scholar
Cleaves, H.J. (2013). Prebiotic chemistry: geochemical context and reaction screening. Life 3(2), 331345.CrossRefGoogle ScholarPubMed
Cornish-Bowden, A. & Cárdenas, M.L. (2008). Self-organization at the origin of life. J. Theor. Biol. 252, 411418.CrossRefGoogle ScholarPubMed
Cronin, J. & Reisse, J. (2005). Chirality and the origin of homochirality. In Lectures in Astrobiology, ed. Gargaud, M., Barbier, B., Martin, H. & Reisse, J., pp. 473515. Springer, Berlin Heidelberg.Google Scholar
Cronin, J.R. & Pizzarello, S. (1997). Enantiomeric excesses in meteoritic amino acids. Science 275, 951955.CrossRefGoogle ScholarPubMed
Ehrenfreund, P. & Cami, J. (2010). Cosmic carbon chemistry: from the interstellar medium to the early Earth. Cold Spring Harb. Perspect. Biol. 2(12), a002097.Google Scholar
Ehrenfreund, P. & Charnley, S. (2000). Organic molecules in the interstellar medium, comets, and meteorites: a voyage from dark clouds to the early earth. Annu. Rev. Astron. Astrophys. 38, 427483.Google Scholar
Eigen, M. (1971). Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58(10), 465523.Google Scholar
Eigen, M. (1993). The origin of genetic information: viruses as models. Gene 135(1), 3747.CrossRefGoogle ScholarPubMed
Fitz, D., Reiner, H., Plankensteiner, K. & Rode, B.M. (2007). Possible origins of biohomochirality. Curr. Chem. Biol. 1, 4152.Google Scholar
Gabb, H.A., Jackson, M.R. & Sternberg, J.E. (1997). Modelling protein docking using shape complementarity, electrostatics and biochemical information. J. Mol. Biol. 272, 106120.Google Scholar
Gleiser, M., Nelson, B.J. & Walker, S.I. (2012). Chiral polymerization in open systems from chiral-selective reaction rates. Orig. Life Evol. Biosph. 42, 333346.CrossRefGoogle ScholarPubMed
Herrera, A.L. (1924). Biología y plasmogenia. Herrero Hermanos, Mexico.Google Scholar
Herrera, A.L. (1942). A new theory of the origin and nature of life. Science 96(2479), 1414.CrossRefGoogle ScholarPubMed
Hordijk, W., Hein, J. & Steel, M. (2010). Autocatalytic sets and the origin of life. Entropy 12, 17331742.CrossRefGoogle Scholar
Israel, D.J. & Perry, J. (1990). What is Information? In Information, Language and Cognition, ed. Hanson, P., pp. 119. Vancouver: University of British Columbia Press.Google Scholar
Janin, J. (1996). Protein-protein recognition. Prog. Biophys. Mol. Biol. 64(2–3), 145166.CrossRefGoogle Scholar
Jheeta, S. (2015). The routes of emergence of Life from LUCA during the RNA and Viral World: a conspectus. Life 5(2), 14451453.Google Scholar
Kaddour, H. & Sahai, N. (2014 ). Synergism and mutualism in non-enzymatic RNA polymerization. Life 4(4), 598620.Google Scholar
Kauffman, S. (1986). Autocatalytic sets of proteins. J. Theor. Biol. 119, 124.CrossRefGoogle ScholarPubMed
Kauffman, S. (1993). Origins of Order: Self-organization and Selection in Evolution. Oxford University Press, USA.Google Scholar
Kauffman, S. (2011). Approaches to the origin of life on Earth. Life 1(1), 3448.Google Scholar
Kawasaki, T., Hatase, K., Fujii, Y., Jo, K., Soai, K. & Pizzarello, S. (2006). The distribution of chiral asymmetry in meteorites: an investigation using asymmetric autocatalytic chiral sensors. Geochim. Cosmochim. Acta 70, 53955402.Google Scholar
Kofler, W. (2014). ‘Information’-from an evolutionary point of view. Information 5(2), 272284.CrossRefGoogle Scholar
Kohlas, J. & Schmid, J. (2014). An algebraic theory of information: an introduction and survey. Information 5(2), 219254.CrossRefGoogle Scholar
Kompanichenko, V.N. (2008). Three stages of the origin-of-life process: bifurcation, stabilization and inversion. Int. J. Astrobiol. 7(1), 2746.CrossRefGoogle Scholar
Kompanichenko, V.N. (2009). Changeable hydrothermal media as a potential cradle of life on a planet. Planet. Space Sci. 57, 468476.CrossRefGoogle Scholar
Kompanichenko, V.N. (2012a). Origin of life by thermodynamic inversion: a universal process. In Genesis–in the Beginning, ed. Seckbach, J., pp. 305320. Springer, Netherlands.Google Scholar
Kompanichenko, V.N. (2012b). Inversion concept of the origin of life. Orig. Life Evol. Biosph. 42, 153178.CrossRefGoogle ScholarPubMed
Kompanichenko, V.N. (2014). Emergence of biological organization through thermodynamic inversion. Front. Biosci. 6, 208224.CrossRefGoogle ScholarPubMed
Larralde, R., Robertson, M.P. & Miller, S.L. (1995). Rates of decomposition of ribose and other sugars: implications for chemical evolution. Proc. Natl. Acad. Sci. U.S.A. 92(18), 81588160.Google Scholar
Leduc, S. (1912). La Biologie Synthétique. A. Poinat, France.Google Scholar
Lehn, J.M. (1990). Perspectives in supramolecular chemistry–from molecular recognition towards molecular information processing and self-organization. Angew. Chem. Int. Ed. Engl. 29(11), 13041319.Google Scholar
Lehn, J.M. (2007). From supramolecular chemistry towards constitutional dynamic chemistry and adaptive chemistry. Chem. Soc. Rev. 36(2), 151160.CrossRefGoogle ScholarPubMed
Lenski, W. (2010). Information: a conceptual investigation. Information 1(2), 74118.CrossRefGoogle Scholar
Lo Conte, L., Chothia, C. & Janin, J. (1999). The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285, 21772198.Google Scholar
Maury, C.P.J. (2009). Self-propagating β-sheet polypeptide structures as prebiotic informational molecular entities: the amyloid world. Orig. Life Evol. Biosph. 39, 141150.Google Scholar
Meierhenrich, U. (2008). A new record for chiral molecules in meteorites. In Amino Acids and the Asymmetry of Life, ed. Meierhenrich, U., pp. 145159. Springer, Berlin Heidelberg.Google Scholar
Micali, M., Engelkamp, H., van Rhee, P.G., Christianen, P.C.M., Monsú Scolaro, L. & Maan, J.C. (2012). Selection of supramolecular chirality by application of rotational and magnetic forces. Nat. Chem. 4(3), 201207.Google Scholar
Nooren, I.M.A. & Thornton, J.M. (2003). Structural characterisation and functional significance of transient protein–protein interactions. J. Mol. Biol. 325, 9911018.CrossRefGoogle ScholarPubMed
Ogayar, A. & Sánchez-Pérez, M. (1998). Prions: an evolutionary perspective. Int. Microbiol. 1, 183190.Google Scholar
Oparin, A.I. & Gladilin, K.L. (1980). Evolution of self-assembly of probionts. Biosystems 12, 133145.Google Scholar
Pablo, C.O. & Sauer, R.T. (1984). Protein-DNA recognition. Annu. Rev. Biochem. 53, 293321.Google Scholar
Palmans, A.R.A. & Meijer, E.W. (2007). Amplification of chirality in dynamic supramolecular aggregates. Angew. Chem. Int. Ed. 46, 89488968.Google Scholar
Peczuh, M.W. & Hamilton, A.D. (2000). Peptide and protein recognition by designed molecules. Chem. Rev. 100(7), 24792494.Google Scholar
Pizzarello, S. (2006). The chemistry of life's origin: a carbonaceous meteorite perspective. Acc. Chem. Res. 39(4), 231237.Google Scholar
Pizzarello, S. (2007). The chemistry that preceded life's origin: a study guide from meteorites. Chem. Biodivers. 4, 680693.Google Scholar
Pizzarello, S. & Cronin, J.R. (2000). Non-racemic amino acids in the Murray and Murchison meteorites. Geochim. Cosmochim. Acta 64(2), 329338.Google Scholar
Pizzarello, S. & Groy, Th.L. (2011). Molecular asymmetry in extraterrestrial organic chemistry: an analytical perspective. Geochim. Cosmochim. Acta 75, 645656.CrossRefGoogle Scholar
Pizzarello, S., Zolensky, M. & Turk, K.A. (2003). Nonracemic isovaline in the Murchison meteorite: chiral distribution and mineral association. Geochim. Cosmochim. Acta 67(8), 15891595.CrossRefGoogle Scholar
Radu, P. (2004). The early history of bio-information. In Between Necessity and Probability: Searching for the Definition and Origin of Life, ed. Radu, P., pp. 95120. Springer, Berlin Heidelberg.Google Scholar
Ribó, J.M., Crusats, J., Sagués, F., Claret, J. & Rubires, R. (2001). Chiral sign induction by vortices during the formation of mesophases in stirred solutions. Science 292, 20632066.Google Scholar
Scott, W.G., Szöke, A., Blaustein, J., O'Rourke, S.M. & Robertson, M.P. (2014). RNA catalysis, thermodynamics and the origin of life. Life 4(2), 131141.CrossRefGoogle ScholarPubMed
Sephton, M.A. (2002). Organic compounds in carbonaceous meteorites. Nat. Prod. Rep. 19, 292311.Google Scholar
Shannon, C.E. (1948). A mathematical theory of communication. Bell Syst. Tech. J. 27, 379423, 623–656.Google Scholar
Shapiro, R. (2000). A replicator was not involved in the origin of life. IUBMB Life 49(3), 173176.Google Scholar
Simonneaux, G., Srour, H., Le Maux, P., Chevance, S. & Carrie, D. (2014). Metalloporphyrin symmetry in chiral recognition and enantioselective catalysis. Symmetry 6, 210221.Google Scholar
Spach, G. & Brack, A. (1979). β-Structures of polypeptides with L- and D-residues. Part II. –Statistical analysis and enrichment in enantiomer. J. Mol. Evol. 13, 4756.Google Scholar
Tamura, K. (2011). Molecular basis for chiral selection in RNA aminoacylation. Int. J. Mol. Sci. 12(7), 47454757.Google Scholar
Trifonov, E.N. (2011). Vocabulary of definitions of life suggests a definition. J. Biomol. Struct. Dyn. 29(2), 259266.CrossRefGoogle ScholarPubMed
Tyagi, N.K., Kumar, A., Goyal, P., Pandey, D., Siess, W. & Kinne, R.K.H. (2007). D-Glucose-recognition and phlorizin-binding sites in human sodium/d-glucose cotransporter 1 (hSGLT1): a tryptophan scanning study. Biochemistry 46, 1361613628.Google Scholar
Varela, F.J., Maturana, H.R. & Uribe, R. (1974). Autopoiesis: the organization of living systems, its characterization and a model. Biosystems 5, 187196.Google Scholar
Williamson, J.R. (2000). Induced fit in RNA–protein recognition. Nat. Struct. Biol. 7(10), 834837.Google Scholar
Woolf, N.J. (2015) A hypothesis about the origin of biology. Orig. Life Evol. Biosph. 45, 257274.Google Scholar
Yang, W., He, H. & Drueckhammer, D.G. (2001). Computer-guided design in molecular recognition: design and synthesis of a glucopyranose receptor. Angew. Chem. Int. Ed. 40(9), 17141718.Google Scholar
Yin, P., Zhang, Z.M., Lv, H., Li, T., Haso, F., Hu, L., Zhang, B., Bacsa, J., Wei, Y., Gao, Y., Hou, Y., Li, Y.G., Hill, C.L., Wang, E.B. & Liu, T. (2015). Chiral recognition and selection during the self-assembly process of protein-mimic macroanions. Nat. Commun. 6: 6475, doi: 10.1038/ncomms7475.Google Scholar