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Early evolution of efficient enzymes and genome organization

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Cellular life with complex metabolism probably evolved during the reign of RNA, when it served as both information carrier and enzyme. Jensen proposed that enzymes of primordial cells possessed broad specificities: they were generalist. When and under what conditions could primordial metabolism run by generalist enzymes evolve to contemporary-type metabolism run by specific enzymes? Results Here we show by numerical simulation of an enzyme-catalyzed reaction chain that specialist enzymes spread after the invention of the chromosome because protocells harbouring unlinked genes maintain largely non-specific enzymes to reduce their assortment load. When genes are linked on chromosomes, high enzyme specificity evolves because it increases biomass production, also by reducing taxation by side reactions. Conclusion The constitution of the genetic system has a profound influence on the limits of metabolic efficiency. The major evolutionary transition to chromosomes is thus proven to be a prerequisite for a complex metabolism. Furthermore, the appearance of specific enzymes opens the door for the evolution of their regulation. Reviewers This article was reviewed by Sándor Pongor, Gáspár Jékely, and Rob Knight.

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Publié le 01 janvier 2012
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Szilágyiet al. Biology Direct2012,7:38 http://www.biologydirect.com/content/7/1/38
R E S E A R C HOpen Access Early evolution of efficient enzymes and genome organization 1,2 1,2,31,2,3* András Szilágyi, Ádám Kunand Eörs Szathmáry
Abstract Background:Cellular life with complex metabolism probably evolved during the reign of RNA, when it served as both information carrier and enzyme. Jensen proposed that enzymes of primordial cells possessed broad specificities: they were generalist. When and under what conditions could primordial metabolism run by generalist enzymes evolve to contemporarytype metabolism run by specific enzymes? Results:Here we show by numerical simulation of an enzymecatalyzed reaction chain that specialist enzymes spread after the invention of the chromosome because protocells harbouring unlinked genes maintain largely nonspecific enzymes to reduce their assortment load. When genes are linked on chromosomes, high enzyme specificity evolves because it increases biomass production, also by reducing taxation by side reactions. Conclusion:The constitution of the genetic system has a profound influence on the limits of metabolic efficiency. The major evolutionary transition to chromosomes is thus proven to be a prerequisite for a complex metabolism. Furthermore, the appearance of specific enzymes opens the door for the evolution of their regulation. Reviewers:This article was reviewed by Sándor Pongor, Gáspár Jékely, and Rob Knight. Keywords:Origin of life, Chromosome, Metabolism, Ribozyme, Major transitions, Enzyme evolution
Background The major evolutionary transitions [1] set a timeline onto which other evolutionary milestones can be inte grated. The emergence of complex metabolism in the RNA world [24] (an age when RNA served as both information carrier and enzyme) is one such mile stone, whose place in the order of events has not yet been determined. Some rudimentary metabolism could have existed on mineral surfaces [5], where RNA oligo mers can also form [6]. Templatebased replication of these oligomers was achieved at this stage, which trans formed RNA molecules into units of evolution. These independent replicators became compartmentalized dur ing the first major evolutionary transition [1], and by their very nature, possessed at least the ability to enhance their own formation. A good fraction of early ribozymes
* Correspondence: szathmary.eors@gmail.com 1 Department of Plant Taxonomy and Ecology, Institute of Biology, Eötvös University, Pázmány Péter sétány 1/C, 1117, Budapest, Hungary 2 Department of Plant Taxonomy and Ecology, Research Group of Ecology and Theoretical Biology, Eötvös University and The Hungarian Academy of Sciences, Pázmány P. sétány 1/C, H1117, Budapest, Hungary Full list of author information is available at the end of the article
(RNA enzymes) was likely to have been inefficient generalists [7], as it must have taken time to optimize their function. Furthermore, the everchanging and unpredict able primordial environment probably favored broad speci ficities and the ability to adapt to new substrates [8]. By the invention of translated protein synthesis [1], a complex me tabolism was likely in place. We can conclude that a metab olism driven by specialist enzymes is likely to have emerged in the RNA world [2], before the invention of the genetic code and translation. Evolution of complex metabolism requires that enzymes be able to evolve from one function to another; and be able to reach high rate enhancement and specificity. The plethora of artificially evolved ribozymes [3,4,9] testify that RNA is well capable of acquiring novel catalytic functions. Furthermore, evolution can lead from one enzyme func tion to another (e.g. the Bartel I ligase that was turned into an RNA polymerase [10,11]). RNA enzymes are capable of very specific catalysis with potentially high catalytic rate enchantment [12]. Thus there is no biochemical reason for not having specific enzymes rather soon after the appearance of ribozymes. The possibility of division of
© 2012 Szilagyi et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.