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Novel Look at DNA and Life-Symmetry As Evolutionary Forcing

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Novel Look at DNA and Life-Symmetry As Evolutionary Forcing Novel look at DNA and life—Symmetry as evolutionary forcing Rosandić, Marija; Vlahović, Ines; Paar, Vladimir Source / Izvornik: Journal of Theoretical Biology, 2019, 483 Journal article, Published version Rad u časopisu, Objavljena verzija rada (izdavačev PDF) https://doi.org/10.1016/j.jtbi.2019.08.016 Permanent link / Trajna poveznica: https://urn.nsk.hr/urn:nbn:hr:217:296602 Rights / Prava: Attribution 4.0 International Download date / Datum preuzimanja: 2021-09-23 Repository / Repozitorij: Repository of Faculty of Science - University of Zagreb Journal of Theoretical Biology 483 (2019) 109985 Contents lists available at ScienceDirect Journal of Theoretical Biology journal homepage: www.elsevier.com/locate/jtb Novel look at DNA and life—Symmetry as evolutionary forcing ∗ Marija Rosandi c´ a,d, Ines Vlahovi c´ b,c, , Vladimir Paar a,b a Croatian Academy of Sciences and Arts, 10 0 0 0 Zagreb, Croatia b Department of Physics, Faculty of Science, University of Zagreb, 10 0 0 0 Zagreb, Croatia c Algebra University College, 10 0 0 0 Zagreb, Croatia d University hospital centre Zagreb (ret.), Zagreb, Croatia a r t i c l e i n f o a b s t r a c t Article history: After explanation of the Chargaffs´ first parity rule in terms of the Watson-Crick base-pairing between the Received 8 February 2018 two DNA strands, the Chargaffs´ second parity rule for each strand of DNA (also named strand symmetry), Revised 21 June 2018 which cannot be explained by Watson-Crick base-pairing only, is still a challenging issue already fifty Accepted 22 August 2019 years. We show that during evolution DNA preserves its identity in the form of quadruplet A + T and Available online 27 August 2019 C + G rich matrices based on purine-pyrimidine mirror symmetries of trinucleotides. Identical symmetries Keywords: are present in our classification of trinucleotides and the genetic code table. All eukaryotes and almost all Chargaff’s second parity rule prokaryotes (bacteria and archaea) have quadruplet mirror symmetries in structural form and frequencies Strand symmetry following the principle of Chargaff’s second parity rule and Natural symmetry law of DNA creation and Trinucleotide classification conservation. Some rare symbionts have mirror symmetry only in their structural form within each DNA Genetic code table strand. Based on our matrix analysis of closely related species, humans and Neanderthals, we find that Entropy the circular cycle of inverse proportionality between trinucleotides preserves identical relative frequencies of trinucleotides in each quadruplet and in the whole genome. According to our calculations, a change in frequencies in quadruplet matrices could lead to the creation of new species. Violation of quadruplet symmetries is practically inconsistent with life. DNA symmetries provide a key for understanding the restriction of disorder (entropy) due to mutations in the evolution of DNA. ©2019 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license. ( http://creativecommons.org/licenses/by/4.0/ ) 1. Introduction ishi and Herai, 2011; Glazebrook and Wallace, 2012; Rosandi c´ et al., 2013a; Rosandi c´ and Paar, 2014; Afreixo et al., 2015 ). Comparative genomic analyses revealed some universals of D.J. Gross expressed a general remark regarding the symmetry genome evolution in the form of nucleotide distributions or principle as the primary feature of nature ( Gross, 1996 ): “We are their specific relationships. The question is whether they re- embarked on a new stage of exploration of fundamental laws of flect some fundamental “laws” of genome evolution or whether nature, a voyage guided largely by the search for the discovery of they are a kind of statistical patterns ( Koonin, 2011 ). The idea new symmetries.” that natural laws are associated with symmetry is present in Jacques Monod attached great significance to symmetry and science, but the symbiosis of mathematics and natural laws function in biological systems. He pointed out that the word is still not fully understood ( Wigner, 1969a ). Emmy Noether symmetry, here, must not be understood in its purely geometrical achieved such spectacular result in 1918 when she proved her connotation, but in the much wider sense ( Monod, 1978 ): “The famous theorem, relating symmetry in time and the energy concept of symmetry becomes almost identical with that of order conservation law ( König and Wiss, 1918; Gross, 1996; Kosmann- within a structure, whether in space or time, or purely in abstracto. Schwarzbach, 2010 ) . The use of the concept of symmetry has The difficulties stem precisely from the extreme complexity of been spreading throughout science, for example Wigner (1969b ), biological order, even though it often does express itself, partially, Muller (20 03) , Mainzer (20 05) , Zee (20 07) , Bindi et al. (2015) , in some very simple and very obvious symmetry elements.” including biology ( Monod, 1978; Bashford et al., 1998; Niko- Chargaff’s second parity rule stating a marked similarity be- lajewa et al., 2005; Kong, 2009; Ramos et al., 2010; Yamag- tween the frequencies of nucleotides and oligonucleotides and those of their respective reverse complements within each strand of sufficiently long ( > 100kb) double stranded DNA, is an inter- ∗ Corresponding author. esting empirical pattern ( Rudner et al., 1968; Prabhu, 1993; Qi E-mail addresses: [email protected] (M. Rosandic),´ [email protected], and Cuticchia, 20 01; Kong, 20 09; Baisnee et al., 2002; Zhang and [email protected] (I. Vlahovi c),´ [email protected] (V. Paar). https://doi.org/10.1016/j.jtbi.2019.08.016 0022-5193/© 2019 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license. ( http://creativecommons.org/licenses/by/4.0/ ) 2 M. Rosandi´ c, I. Vlahovi´ c and V. Paar / Journal of Theoretical Biology 483 (2019) 109985 Huang, 2008; Perez, 2010; Sobottka and Hart, 2011; Mascher et al., genome? The Watson-Crick rule, binding purine from one strand 2013; Rapoport and Trifonov, 2013; Rosandi c´ et al., 2013b; Zhang and pyrimidine from the other, A ↔ T, G ↔ C, does not provide an et al., 2013 ). This rule generally holds for double stranded DNA answer to these questions because Watson-Crick pairing does not genomes, with the exception of some rare DNA symbionts, single- occur within the same strand of DNA. stranded genomes and organelles ( Mitchell and Bridge, 2006; Nikolau and Almirantis, 2006 ). 2. Quadruplet classification of trinucleotides Chargaff’s first parity rule for pairs of A-T and C-G nu- cleotides between strands ( Chargaff, 1951 ) was fully explained by The basic role of DNA is related to the genetic code. Its con- the Watson-Crick pairing in the DNA double helix ( Watson and stituents in coding DNA are codons and, therefore, in noncoding Crick, 1953 ). sequences, we consider trinucleotides as basic entities. Thus, the On the other hand, in spite of several proposals, a definitive ex- four different nucleotides (A, T, C and G) provide 64 possible trin- planation of Chargaff’s second parity rule has not been fully ac- ucleotide combinations, which are usually classified alphabetically. cepted yet. Its fundamental cause is still somewhat controversial Because the alphabetical ordering is purely artificial, without any ( Baisnee et al., 2002; Zhang and Huang, 2008; Mascher et al., 2013; biological background, it cannot reveal any biochemical correla- Rapoport and Trifonov, 2013; Forsdyke and Bell, 2004; Chen and tions. Zhao, 2005; Albrecht-Buehler, 2006, 2007; Okamura et al., 2007; Our quadruplet classification of trinucleotides is based on the Kong, 2009; Rosandi c´ et al., 2016; Afreixo et al., 2016 ). It was sug- following: each trinucleotide (denoted D ) belongs to its quadru- gested that Chargaff’s second parity rule could probably exist from plet consisting of direct (D) - reverse complement (RC) - comple- the very beginning of genome evolution. Information emerging ment (C) - reverse (R) trinucleotides ( Table 1 ). For example, the from modern genome structures, in terms of small oligonucleotide quadruplet corresponding to the ATG trinucleotide is: ATG (D), TAC frequencies could be helpful for the reconstruction of the primor- (C), GTA (R), and CAT (RC). If the TAC trinucleotide within the dial genome as well as for further understanding of the pattern of same quadruplet is chosen as direct, then the other three mem- genome evolution. This information could shed light on the ori- bers of the quadruplet are ATG (C), CAT (R) and GTA (RC). Thus gin of genomes, and even on the origin of life ( Zhang et al., 2013 ). each quadruplet consists of the same four trinucleotides, regardless Thus, it was noted that Chargaff’s second parity rule could reveal of which of the four is taken as direct, and none of them belong to general species-independent properties and have implications of any of the other quadruplets. some unknown mechanism that is likely to be present ( Albrecht- We constructed the classification of trinucleotides from two Buehler, 2007; Rapoport and Trifonov, 2013 ). quadruplet groups: ten A + T rich and ten C + G rich ( Rosandi c´ et al., As a basic feature of genomic sequences, oligonucleotide (in 2013b, 2016 ), which encompass all 64 trinucleotides ( Table 1 ). To particular trinucleotide) frequency profiles have been used in each member of A + T rich quadruplet belongs a member from C + G studying genome evolution ( Sobottka and Hart, 2011; Albrecht- rich quadruplet due to purine-pyrimidine transformation within Buehler, 20 06, 20 07; Rosandi c´ et al., 2016; Afreixo et al., 2016; the A, C and T, G amino-keto pairs: A →C, C →A and T → G, G → T. In Zhang and Wang, 2011, 2012 ) . Regarding the importance of trinu- this way, both A + T rich and C + G rich groups are segmented into cleotides in the whole genomic sequences, new evidence was re- three subgroups: 1) nonsymmetrical trinucleotides, each consisting cently provided for their fundamental role in evolution ( Frenkel of three different nucleotides, 2) nonsymmetrical trinucleotides, and Trifonov, 2012; Frenkel et al., 2013 ).
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