Abstract
BackgroundFundamental problems faced by the protocells and their modern descendants include how to go from one phenotypic state to another; escape from a basin of attraction in the space of phenotypes; reconcile conflicting growth and survival strategies (and thereby live on ‘the scales of equilibria’); and create a coherent, reproducible phenotype from a multitude of constituents.Presentation of the hypothesisThe solutions to these problems are likely to be found with the organic and inorganic molecules and inorganic ions that constituted protocells, which we term SUMIs for Simple Universal Molecules and Ions. These SUMIs probably included polyphosphate (PolyP) as a source of energy and of phosphate; poly-(R)-3-hydroxybutyrate (PHB) as a source of carbon and as a transporter in association with PolyP; polyamines as a source of nitrogen; lipids as precursors of membranes; as well as peptides, nucleic acids, and calcium. Here, we explore the hypothesis that the direct interactions between PHB, PolyP, polyamines and lipids – modulated by calcium – played a central role in solving the fundamental problems faced by early and modern cells.Testing the hypothesisWe review evidence that SUMIs (1) were abundant and available to protocells; (2) are widespread in modern cells; (3) interact with one another and other cellular constituents to create structures with new functions surprisingly similar to those of proteins and RNA; (4) are essential to creating coherent phenotypes in modern bacteria. SUMIs are therefore natural candidates for reducing the immensity of phenotype space and making the transition from a “primordial soup” to living cells.Implications of the hypothesisWe discuss the relevance of the SUMIs and their interactions to the ideas of molecular complementarity, composomes (molecular aggregates with hereditary properties based on molecular complementarity), and a prebiotic ecology of co-evolving populations of composomes. In particular, we propose that SUMIs might limit the initial phenotype space of composomes in a coherent way. As examples, we propose that acidocalcisomes arose from interactions and self-selection among SUMIs and that the phosphorylation of proteins in modern cells had its origin in the covalent modification of proteins by PHB.ReviewersThis article was reviewed by Doron Lancet and Kepa Ruiz-Mirazo.
Highlights
Fundamental problems faced by the protocells and their modern descendants include how to go from one phenotypic state to another; escape from a basin of attraction in the space of phenotypes; reconcile conflicting growth and survival strategies; and create a coherent, reproducible phenotype from a multitude of constituents.Presentation of the hypothesis: The solutions to these problems are likely to be found with the organic and inorganic molecules and inorganic ions that constituted protocells, which we term SUMIs for Simple Universal Molecules and Ions
We propose that acidocalcisomes arose from interactions and self-selection among SUMIs and that the phosphorylation of proteins in modern cells had its origin in the covalent modification of proteins by PHB
Presentation of the hypothesis The primary hypothesis that we present here is that composomes and their functions evolved by means of a series of SUMIs that endowed prebiotic ecologies with unprecedented ways: to control ion fluxes and osmotic pressure gradients; to store carbon, nitrogen and phosphate, and to store and release energy; to select interacting molecules; to catalyze reactions and to generate polymers
Summary
The problem of how life might be created on Earth was solved somehow during the evolution of the distant ancestors of modern cells. Interactions between phospholipids and the nascent peptides generated via coupling between transcription, translation and protein insertion into membrane are considered to structure the membrane into domains that help determine the phenotype [67] Such interactions are a prime example of the importance of molecular complementarity. In the quest for solutions to the fundamental problem of generating coherent phenotypes, it could be argued that calcium was wellplaced right from the start to play a unifying role by interacting directly or indirectly with PolyP, PHB, polyamines and phospholipids. This role continues in modern cells where calcium helps coordinate membrane and cytoskeletal structures, enzymic activity, and kinases and phosphatases. Author details 1Department of Biology, University of Rouen, 76821 Mont Saint Aignan, France. 2Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA. 3Amine Pharma Research Institute, Innovation Plaza at Chiba University, 1-8-15 Inohana, Chuo-ku, Chiba 260-0856, Japan. 4Department of Physiology, Michigan State University, East Lansing, MI 48824, USA
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