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From Compositional Chemical Ecologies to Self-replicating Ribosomes and on to Functional Trait Ecological Networks

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Evolutionary Biology

Abstract

In contrast to theories arguing that cellular life has evolved to transmit genes, we propose instead that cellular life evolved to facilitate the full potential of self-replicating ribosomes. Our theory explicitly rejects “master molecule” theories such as Dawkins’s “selfish gene” in favor of the emergence of life by means of systems of increasingly networked interactions that carried out metabolic and genetic functions concurrently within a complex chemical ecology. The critical role of networking chemical interactions within this ecology was (as it still is) mediated by all possible forms of molecular complementarity, of which base-pairing in RNA and DNA is just one. Selection for molecular complementarity functional and structural modules vastly increased the probability that networked systems would evolve, eventually resulting in the first self-replicating entity, which we believe was the ribosome. We make six predictions from our ribosome-first theory of cellular evolution that may seem, at first glance, heretical: (1) Ribosomal RNA (rRNA) contains genetic information encoding its own proteins, meaning that it also encodes messenger RNA (mRNA); (2) these proteins bind to the rRNA to form the functional ribosomal structure, but since the rRNA is also functioning as mRNA, the ribosomal proteins must bind to their own mRNA as well; (3) rRNA encodes all of the transfer RNAs (tRNA) required for the translation of its genetic information; (4) thus, tRNAs may be the precursor modules that gave rise to rRNA; (5) rRNA is pleiofunctional, integrating genetic, protein, translational, and structural information often in the same or overlapping sequences and in all reading frames; and (6) since the ribosome gave rise to cellular life, tRNA- and rRNA-like genetic information must be major building blocks from which cellular genomes evolved. We present evidence supporting all six of these apparently unlikely predictions. Our conclusion is that life is not about the evolution of genes, but the evolution of the kinds of networked interactions through complementarity that characterize ecologies: Genes evolved merely as storage units to “back up” ribosomal functions. This same complementarity-based approach may help to explain why functional traits, rather than genetic populations, appear to network interactions within higher-order systems such as ecosystems and holobionts.

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Acknowledgements

We would like to thank the US National Science Foundation for granting support and Professors Patrick F. Dillon and Adam W. Brown of Michigan State University and Professors Vic Norris and Corinne Loutellier-Bourhis of the University of Rouen, as well as two of our students, Tyler Rhinesmith and Andrew Baker, for their invaluable assistance and their feedback during the development of this research.

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Authors and Affiliations

  1. Department of Physiology, Michigan State University, East Lansing, MI, 48824, USA

    Robert Root-Bernstein

  2. Department of Bioscience, Aarhus University, Aarhus, Denmark

    Meredith Root-Bernstein

  3. Institute of Ecology and Biodiversity, Santiago, Chile

    Meredith Root-Bernstein

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  1. Robert Root-Bernstein
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Correspondence to Robert Root-Bernstein .

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  1. CNRS, Laboratoire Evolution Biologique et Modélisation, Université d’Aix-Marseille, Marseille, France

    Pierre Pontarotti

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Root-Bernstein, R., Root-Bernstein, M. (2016). From Compositional Chemical Ecologies to Self-replicating Ribosomes and on to Functional Trait Ecological Networks. In: Pontarotti, P. (eds) Evolutionary Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-41324-2_19

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