Molecular shape as a key source of prebiotic information

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Highlights

  • Molecular shape plays a key role in the origin of life.

  • Spatial information in the molecular recognition of living systems is biological information.

  • Spatial information as part of the central dogma of molecular biology.

Abstract

One of the most striking features of a living system is the self-sustaining functional inner organization, which is only possible when a source of internal references is available from which the system is able to self-organize components and processes. Internal references are intrinsically related to biological information, which is typically understood as genetic information. However, the organization in living systems supports a diversity of intricate processes that enable life to endure, adapt and reproduce because of this organization. In a biological context, information refers to a complex relationship between internal architecture and system functionality. Nongenetic processes, such as conformational recognition, are not considered biological information, although they exert important control over cell processes. In this contribution, we discuss the informational nature in the recognition of molecular shape in living systems. Thus, we highlight supramolecular matching as having a theoretical key role in the origin of life. Based on recent data, we demonstrate that the transfer of molecular conformation is a very likely dynamic of prebiotic information, which is closely related to the origin of biological homochirality and biogenic systems. In light of the current hypothesis, we also revisit the central dogma of molecular biology to assess the consistency of the proposal presented here. We conclude that both spatial (molecular shape) and sequential (genetic) information must be represented in this biological paradigm.

Introduction

A fundamental property in living systems is the ability to self-sustain its own organization. This self-sustaining organization needs a source of internal references (data) about the architecture and the functionality supported by the system configuration. To this end, genes are the evident source of the information that regulates living systems. Although information is a context-dependent concept (Tsokolov, 2009), it has been used in biology to describe the complex relationship between the internal organization and the functionality of living beings. Currently, there is no unique definition of information, which is an initial problem for the study of the origins of life. In addition, terms such as genetic information are important notions useful for understanding biological processes. Therefore, with the aim of extending the notion of information to biology, five common criteria cited in the majority of the theories about this concept are identified (Cruz-Rosas et al., 2017). Accordingly, information is a recognizable property whereby i) there exists a (self-) controlled system development; ii) there are dynamics that make possible the discrimination of components; i.e., there is a reduction of uncertainty; iii) there are processes, objects or symbols that represent other processes, objects or symbols; i.e., they have a meaning in the system such that iv) there is an interpretation or understanding of these kinds of processes, objects or symbols; and v) the set of references regarding the previous processes and patterns (i.e., the meaning) can be transmitted and stored because it exerts influence on the formation or transformation of other patterns in the system. These criteria can be obviously found in genetic information. Here, molecular strings are used to encrypt information in such a way that it is available at several points throughout the existence of the system. Additionally, molecular strings are specifically deciphered from locations in the genetic polymer to control (particular) internal processes and the system response to the milieu. However, the point of this study is to show that genetic information is not the only kind of information on which the organization of life is based (Cruz-Rosas et al., 2017, Dickins and Rahman, 2012, Godfrey-Smith and Sterelny, 2016, Rashevsky, 1955).

The processes and organization of living systems are not only under genetic control (Woolf, 2015). The arrangement of the cell membrane, the recognition of substrates and ligands, and epigenetic mechanisms are examples of non-genetically controlled processes (Cavalier-Smith, 2010, Wickner et al., 2007). The theory of autopoiesis states that life is organized through the self-production and self-replacement of its own constituents and the component-functions such that the system can be maintained for longer than its isolated parts (Luisi, 2003, Varela et al., 1974). Genetic information is mainly relevant for the self-production of components, while supramolecular recognition seems to be related mainly to the self-replacement and topological organization of system constituents (molecules or groups of cells) (Jablonka and Raz, 2009). These dual sources do not imply that each type of information in a living system is mutually exclusive; instead, both are present in a conspicuous/hidden mutual association. We identify two modes of information in biological context: The cryptic information, codified in sequences, as in the genes. As well as the explicit information that does not require a transducer by which the encoded-meaning is deciphered to exert control in the system. In explicit information, the references are directly available for use by components. Therefore, explicit information is spatial information (supported by the dynamic transfer of geometries or molecular conformations, similar to a mold that explicitly transfers shape, a process that resembles that of prions during propagation), or temporal information (supported by the acquisition and transfer of references from periodic succession of well-defined steps in a phenomenon).

Information encoded in sequences (molecular strings) is a multistep process in which each monomer must be added to the concatenation at a specific location during a series of events, similar to a token in a script. Moreover, supramolecular recognition also constitutes a dynamic of an informational nature in which the explicit understanding of the molecular shape allows control over the system. This geometric recognition reduces the uncertainty between the molecular conformations that represent the prevailing conditions that have shaped them and induce specific processes in living systems. By limiting biological information to strict genetic information, the other important flow of information, which is based on supramolecular matching and shape recognition, is not considered. Biological information based exclusively on genetic information leads to conceptual barriers and theoretical restrictions in the study of the origin of life.

In the search for self-replicating systems, the focus on replicating sequences of polymers has been overemphasized (Banfalvi, 2019, Szostak, 2017). From an exclusive view of cryptic information, only genetic-like polymers are relevant, but in the scope of a general notion of biological information, polymers such as peptides are also information-carrying molecules. Self-replication can also be explored by means of explicit information. When explicit information is considered, the sequences in polymers are not disregarded, but the information that is transferred is that contained in the molecular shape (its conformation).

In the scenarios of the origin of life, random sequences hardly support an informational dynamic because they depend on the occurrence of the same succession of events (i.e., the same order in the polymerization). Not all sequences are information-carrying sequences: only those that have meaning are considered informational unities (each in its own context). When an information-carrying unity is stabilized in a self-organizing dynamic (self-replicating a sequence), coupling it to another information-carrying unity is difficult (Kauffman, 2011, Silvestre and Fontanari, 2008, Szostak et al., 2016) because sequence-codified information requires a very complicated arrangement that is highly sensitive to external perturbations, including those created through interactions with other informational units. An alternative to multistep processes is the one-step process (Woolf, 2015). Specifically, the dynamics of molecular shape recognition are based on a one-step event in which each supramolecular matching is independent of the others. Dynamics such as this can support a real flow of information, such as that contained in molecular conformation.

The propagation of robust conformations (which are resistant under diverse environmental conditions) gives stability to the system architecture. Prebiotic systems could have been favored by this kind of dynamics. Dissemination of these conformations could take place through the flow of spatial information by means of matching and propagating the molecular shape. The structural maintenance of system unity and the contribution to a prebiotic cradle for the subsequent emergence of information codified in sequences of (genetic-like) polymers are direct consequences of dissemination of enduring conformations. In this theoretical context, we present evidence to support our assumption about the informational nature of the supramolecular dynamics of matching and recognition of molecular shape. In our discussion below, we assume the availability of molecules to form polymers and we cite many studies of the properties of molecules similar to those found in extant organisms. Very little attention has been paid to how molecules of such complexity would arise spontaneously from simple molecules such as CO2, NH3, H2O, (e.j. (Muñoz Caro et al., 2002)) but the properties that these molecules exhibit should be similar enough to what might really occur that useful conclusions may be inferred.

Section snippets

Statements and discussion

We first show that the sources of information at the cellular level of organization are not restricted to genetic information. Accordingly, we discuss the evidence to consider the processes of transfer and recognition of molecular shape as a dynamic of (explicit) spatial information in living systems. Therefore, we show that the transfer of molecular conformations is a very likely source of prebiotic information that is closely related to the origin of biological homochirality and biogenic

CRediT authorship contribution statement

Hugo I. Cruz-Rosas: Conceptualization, Investigation, Writing - original draft, Writing - review & editing, Visualization, Supervision, Funding acquisition. Francisco Riquelme: Investigation, Writing - original draft, Writing - review & editing, Visualization. Alejandra Ramírez-Padrón: Investigation, Writing - original draft, Writing - review & editing, Visualization. Thomas Buhse: Investigation, Writing - review & editing, Visualization. Germinal Cocho: Investigation, Writing - review &

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We are deeply grateful to Professor G Cocho, who passed away while this manuscript was being prepared, his research and mentoring were essential to this paper. This work was financially supported by the DGAPA-UNAM postdoctoral fellowship to HI Cruz-Rosas and partially by the PAPIIT-UNAM project IN108318. We thank Professor Mark Chaplain and the two anonymous reviewers whose comments were very helpful in improving this document.

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