Nonenzymatic, Template‐Free Polymerization of 3’,5’ Cyclic Guanosine Monophosphate on Mineral Surfaces

Abstract

Previous studies on the polymerization of 3',5' cyclic guanosine monophosphate (cGMP) demonstrated the potential of the compound in the abiotic generation of the first oligonucleotide sequences on the early Earth. These experiments were conducted under idealized laboratory conditions, which logically raises the question whether the same chemistry could take place in the harsh environment present on our planet in its earliest days. In the current study, we focus on the mineralogical context of this chemistry and show that numerous, but not all, common minerals assumed to be present on the early Earth could host the polymerization of H-form 3',5' cGMP. In particular, we have found that quartz varieties are especially suitable for this purpose, similar to andalusite, amphibole or micas. On the contrary, olivine, calcite, and serpentine-group minerals interfere with the studied polymerization chemistry. Our results show that crystallization on mineral surfaces, which is mainly a diffusion controlled process, determines the ability of 3',5' cGMP to polymerize. The observation that numerous amorphous and crystalline SiO 2 forms are compatible with the oligomerization chemistry suggests that the process could commonly occur in a wide range of primordial environments allowing for crystallization of the cyclic monomers from a dropping solution.

Influence of Silicate Rock Glass Compositions on the Efficacy of Prebiotic RNA Polymerization Reactions: The Case of 3’,5’ Cyclic Guanosine Monophosphate

“…Similar to our previous observations made on mineral surfaces, [9] crystallinity of the monomers deposited on the studied glasses qualitatively correlates with the amount and length of oligomerization products formed upon subsequent heat-treatment of the dry material for both sets of glasses. Thus, our denaturing gel electrophoresis (Figure 1, to the left) demonstrates that oligoG sequences up to the length of 15 nucleotide units readily form on three of the studied synthetic glasses (labelled as 1, 2 and 5, for compositional data see Table 1).…”

“…This might be the reason for the lowered bulk basicity of these minerals observed in our preceding study. [9] The trends observed for the ability of 3',5'cGMP monomers to polymerize on the studied synthetic glasses agree with those previously reported for silicate minerals. This suggests that (i) amorphous and crystalline silicate surfaces of a given composition are both well suited to serve as support materials for this reaction, and (ii) the overall chemical composition alone strongly determines the effect of silicate rocks, glasses and minerals on the polymerization of 3',5'cGMP.…”

“…The procedure involved deposition of small droplets (2-5 μL) of 1 mM 3',5'cGMP (free acid form) solution on the synthetic glasses. [9] The process was repeated 20-30 times, to enable accumulation of the deposited material in quantities necessary for crystallization. For technical details of the experiment see the Experimental Section.…”

“…Previously, we have shown that polymerization of 3',5' cyclic guanosine monophosphate (3',5'cGMP) is feasible only on those mineral surfaces where the nucleotide monomers can accumulate in a neutral free acid form. [9] This is because the neutral monomers capably self-assemble to an ordered crystalline material that ensures favorable steric conditions for a solid-phase oligomerization reaction. We identified a series of solid surfaces (e. g. amorphous and crystalline SiO 2 forms, some micas and amphiboles) that enable oligomer production from 3',5'cGMP.…”

Rolling circle RNA synthesis catalyzed by RNA

“…Such hypotheses of an ‘RNA world’—a primordial biology centered on RNA as the main biomolecule—are in accord with the essential role of RNA catalysis in present-day biology ( Cech, 2000 ; Goldman and Kacar, 2021 ; Nissen et al, 2000 ; Wilkinson et al, 2020 ) and the discovery of multiple prebiotic synthetic pathways to several of the RNA (and DNA) nucleotides ( Becker et al, 2019 ; Kim et al, 2020 ; Patel et al, 2015 ; Powner et al, 2009 ; Xu et al, 2020 ). In addition, progress in both non-enzymatic ( Deck et al, 2011 ; Hassenkam et al, 2020 ; Prywes et al, 2016 ; Rajamani et al, 2008 ; Sosson et al, 2019 ; Sponer et al, 2021 ; Wachowius and Holliger, 2019 ; Zhang et al, 2020 ; Zhou et al, 2020 ) and RNA-catalyzed polymerization of RNA and some of its analogs ( Attwater et al, 2018 ; Attwater et al, 2013 ; Cojocaru and Unrau, 2021 ; Ekland and Bartel, 1996 ; Horning and Joyce, 2016 ; Johnston et al, 2001 ; Mutschler et al, 2018 ; Shechner et al, 2009 ; Tagami et al, 2017 ; Tjhung et al, 2020 ) is beginning to map out a plausible path to RNA self-replication; a cornerstone of the RNA world hypothesis.…”