The emergence of DNA in the RNA world: an in silico simulation study of genetic takeover

Ma et al. BMC Evolutionary Biology (2015) 15:272 DOI 10.1186/s12862-015-0548-1 RESEARCH ARTICLE Open Access The emergence of DNA in the RNA world: an in silico simulation study of genetic takeover Wentao Ma1*, Chunwu Yu2, Wentao Zhang2, Sanmao Wu1 and Yu Feng1 Abstract Background: It is now popularly accepted that there was an “RNA world” in early evolution of life. This idea has a direct consequence that later on there should have been a takeover of genetic material – RNA by DNA. However, since genetic material carries genetic information, the “source code” of all living activities, it is actually reasonable to question the plausibility of such a “revolutionary” transition. Due to our inability to model relevant “primitive living systems” in reality, it is as yet impossible to explore the plausibility and mechanisms of the “genetic takeover” by experiments. Results: Here we investigated this issue by computer simulation using a Monte-Carlo method. It shows that an RNA-by-DNA genetic takeover may be triggered by the emergence of a nucleotide reductase ribozyme with a moderate activity in a pure RNA system. The transition is unstable and limited in scale (i.e., cannot spread in the population), but can get strengthened and globalized if certain parameters are changed against RNA (i.e., in favor of DNA). In relation to the subsequent evolution, an advanced system with a larger genome, which uses DNA as genetic material and RNA as functional material, is modeled – the system cannot sustain if the nucleotide reductase ribozyme is “turned off” (thus, DNA cannot be synthesized). Moreover, the advanced system cannot sustain if only DNA’s stability, template suitability or replication fidelity (any of the three) is turned down to the level of RNA’s. Conclusions: Genetic takeover should be plausible. In the RNA world, such a takeover may have been triggered by the emergence of some ribozyme favoring the formation of deoxynucleotides. The transition may initially have been “weak”, but could have been reinforced by environmental changes unfavorable to RNA (such as temperature or pH rise), and would have ultimately become irreversible accompanying the genome’s enlargement. Several virtues of DNA (versus RNA) – higher stability against hydrolysis, greater suitability as template and higher fidelity in replication, should have, each in its own way, all been significant for the genetic takeover in evolution. This study enhances our understandings of the relationship between information and material in the living world. Keywords: Origin of life, Molecular evolution, Computer modeling Background In modern organisms, DNA is the major genetic material and protein is the major functional material, both seeming indispensible. Thus, there is a dilemma for the evolution of life: “Which came first, DNA or proteins?” The RNA world hypothesis provided a possible solution to this problem: in some early stage of life, there is neither DNA nor protein but only RNA, acting as both genetic material and functional material [1]. The RNA * Correspondence: 1 College of Life Sciences, Wuhan University, Wuhan 430072, P.R.China Full list of author information is available at the end of the article world hypothesis has gain more and more supporting evidence, and has become the most popular idea in the field of the origin of life [2–5]. Indeed, in reality, peptides are likely to have existed in the RNA world, considering that they may have been easy to synthesize prebiotically and may have been able to aid RNA’s function by forming complexes with RNA [6, 7]. However, these peptides, synthesized abiotically, cannot reappear in the next generation anyway (unlike those encoded proteins emerging later). Thus, the stage was still an “RNA world”, considering chemical existence is not sufficient to “justify” the existence of a substance in a living world (more or less, the peptides can be seen as merely © 2015 Ma et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ma et al. BMC Evolutionary Biology (2015) 15:272 environmental factors, like metal ions, for example). Recently, a significant study suggested that precursors of RNA, proteins and lipids may have derived by common chemistry [8] – while the result was inspiring for researchers working in the field of the origin of life, a clear notion concerning the difference between chemical existence and biotic existence, like mentioned here, becomes particularly important. As a clear consequence of the scenario concerning the RNA world, DNA and proteins (encoded) should have appeared afterwards. For the emergence of DNA, there would be a problem of “genetic takeover”; for the emergence of proteins, there would be a problem of “functional takeover”. Indeed, “after RNA, which came first, DNA or proteins?” is still a question (e.g., [9] and [10]). While problems concerning such critical transitions remain difficult to tackle experimentally, they begin to appear within the reach of computer simulation researches. The present computer simulation study focuses on the genetic takeover and follows the idea of DNA emerging before proteins. Perhaps the authors’ own opinions about the emerging order of DNA and proteins are not important here, and the choice could simply be technical: the genetic takeover is simpler in principle than the functional takeover given that RNA and DNA share the same mechanism in their synthesis, i.e., by base pairing (unlike that in proteins’ synthesis). In particular, we have conducted a series of computer simulation studies concerning the scenario of early development of the RNA world, including the emergence of several important ribozymes [11–13], the cooperation of these ribozymes [14], and the emergence of an RNA “chromosome” (with linked genes coding for the ribozymes) [15]. In fact, it is now feasible, by a slight extension of the approach along this line, to investigate “the emergence of a DNA chromosome” – ultimately, the transition from an RNA world to a DNA/RNA world. Indeed, for this transition to occur, additional functions concerning new kinds of template-directed copying should be required, i.e., the cross copying between DNA and RNA as well as DNA’s replication. However, these new kinds of copying may have been initially catalyzed by that “old” ribozyme, i.e., the ribozyme that catalyzed RNA’s own replication (the “RNA replicase” – “Rep” for short) [2, 16], given the similar chemistry behind a (...truncated)