The Central Symbiosis of Molecular Biology: Molecules in Mutualism

Journal of Molecular Evolution, Aug 2017

As illustrated by the mitochondrion and the eukaryotic cell, little in biology makes sense except in light of mutualism. Mutualisms are persistent, intimate, and reciprocal exchanges; an organism proficient in obtaining certain benefits confers those on a partner, which reciprocates by conferring different benefits. Mutualisms (i) increase fitness, (ii) inspire robustness, (iii) are resilient and resistant to change, (iv) sponsor co-evolution, (v) foster innovation, and (vi) involve partners that are distantly related with contrasting yet complementary proficiencies. Previous to this work, mutualisms were understood to operate on levels of cells, organisms, ecosystems, and even societies and economies. Here, the concepts of mutualism are extended to molecules and are seen to apply to the relationship between RNA and protein. Polynucleotide and polypeptide are Molecules in Mutualism. RNA synthesizes protein in the ribosome and protein synthesizes RNA in polymerases. RNA and protein are codependent, and trade proficiencies. Protein has proficiency in folding into complex three-dimensional states, contributing enzymes, fibers, adhesives, pumps, pores, switches, and receptors. RNA has proficiency in direct molecular recognition, achieved by complementary base pairing interactions, which allow it to maintain, record, and transduce information. The large phylogenetic distance that characterizes partnerships in organismal mutualism has close analogy with large distance in chemical space between RNA and protein. The RNA backbone is anionic and self-repulsive and cannot form hydrophobic structural cores. The protein backbone is neutral and cohesive and commonly forms hydrophobic cores. Molecules in Mutualism extends beyond RNA and protein. A cell is a consortium of molecules in which nucleic acids, proteins, polysaccharides, phospholipids, and other molecules form a mutualism consortium that drives metabolism and replication. Analogies are found in systems such as stromatolites, which are large consortia of symbiotic organisms. It seems reasonable to suggest that ‘polymers in mutualism relationships’ is a useful and predictive definition of life.

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The Central Symbiosis of Molecular Biology: Molecules in Mutualism

The Central Symbiosis of Molecular Biology: Molecules in Mutualism Kathryn A. Lanier 0 1 2 Anton S. Petrov 0 1 2 Loren Dean Williams 0 1 2 RNA Protein Proficiency 0 1 2 Translation Mutualism 0 1 2 0 School of Chemistry and Biochemistry, Georgia Institute of Technology , Atlanta, GA 30332-0400 , USA 1 Kathryn A. Lanier 2 & Loren Dean Williams As illustrated by the mitochondrion and the eukaryotic cell, little in biology makes sense except in light of mutualism. Mutualisms are persistent, intimate, and reciprocal exchanges; an organism proficient in obtaining certain benefits confers those on a partner, which reciprocates by conferring different benefits. Mutualisms (i) increase fitness, (ii) inspire robustness, (iii) are resilient and resistant to change, (iv) sponsor co-evolution, (v) foster innovation, and (vi) involve partners that are distantly related with contrasting yet complementary proficiencies. Previous to this work, mutualisms were understood to operate on levels of cells, organisms, ecosystems, and even societies and economies. Here, the concepts of mutualism are extended to molecules and are seen to apply to the relationship between RNA and protein. Polynucleotide and polypeptide are Molecules in Mutualism. RNA synthesizes protein in the ribosome and protein synthesizes RNA in polymerases. RNA and protein are codependent, and trade proficiencies. Protein has proficiency in folding into complex three-dimensional states, contributing enzymes, fibers, adhesives, pumps, pores, switches, and receptors. RNA has proficiency in direct molecular recognition, achieved by complementary base pairing interactions, which allow it to maintain, record, and transduce information. The large phylogenetic distance that characterizes partnerships in organismal mutualism has close analogy with large distance in chemical space between RNA and protein. The The Central Dogma of Molecular Biology Origin of life; Co-evolution; Assembly - RNA backbone is anionic and self-repulsive and cannot form hydrophobic structural cores. The protein backbone is neutral and cohesive and commonly forms hydrophobic cores. Molecules in Mutualism extends beyond RNA and protein. A cell is a consortium of molecules in which nucleic acids, proteins, polysaccharides, phospholipids, and other molecules form a mutualism consortium that drives metabolism and replication. Analogies are found in systems such as stromatolites, which are large consortia of symbiotic organisms. It seems reasonable to suggest that ‘polymers in mutualism relationships’ is a useful and predictive definition of life. Introduction Beyond the root of the tree of life lays the origin. During the origin of life, the onset of protein coding led to complex macromolecular structures and functions. The translation of mRNA into protein, catalyzed by the ribosome, set the path of biology that has dominated the biological earth for over 3.8 billion years. The overwhelming complexity of life rests on simple principles. Natural selection over vast time, from a common ancestor to the present, generated great diversity. The Central Dogma (Crick 1970) constrains living systems to well-defined pathways of information flow among a small number of biopolymer types (Fig. 1). Each of these linear biopolymers is formed by condensation dehydration reactions among modest sets of monomer units (Voet and Voet 2011) . Biological information is represented by sequences of linked monomer units. Molecules in Mutualism: A Unifying Principle The goal here is to extend important principles of biology to underlying molecules, extending the scope and explanatory power. We believe structure, function, and evolution of biopolymers are explained and best-described by their relationships with each other. RNA and protein are Molecules in Mutualism. This defining principle of biology and biochemistry has explanatory power comparable to the Central Dogma. Molecules in Mutualism is a rigorous and predictive definition of life. What is Mutualism? A mutualism (Fig. 2) is a persistent and intimate interaction that benefits partnering species (Douglas 2015) . Mutualism is reciprocal exchange; a species proficient in obtaining certain benefits confers those onto a partner, which reciprocates by conferring different benefits (Schwartz and Hoeksema 1998) . Mutualisms are everywhere in the biosphere and are fundamentally important in evolution and ecology (Bronstein 2015) . Mutualisms (i) sponsor co-evolution, (ii) foster innovation, (iii) increase fitness, (iv) inspire robustness, (v) are resilient and resistant to change, and (vi) involve partners that are distantly related with contrasting yet complementary proficiencies. Levels of Mutualism Mutualisms are understood to operate on levels of cells, organisms, ecosystems, and even societies and economies. The eukaryotic cell is a culmination of mutualism between simpler prokaryotic cells (Sagan 1967; Poole and Gribaldo 2014; Gray 2017) . The m (...truncated)


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Kathryn A. Lanier, Anton S. Petrov, Loren Dean Williams. The Central Symbiosis of Molecular Biology: Molecules in Mutualism, Journal of Molecular Evolution, 2017, pp. 1-6, DOI: 10.1007/s00239-017-9804-x