Abstract
Membraneless compartments, such as complex coacervates, have been hypothesized as plausible prebiotic micro-compartments due to their ability to sequester RNA; however, their compatibility with essential RNA World chemistries is unclear. We show that such compartments can enhance key prebiotically-relevant RNA chemistries. We demonstrate that template-directed RNA polymerization is sensitive to polycation identity, with polydiallyldimethylammonium chloride (PDAC) outperforming poly(allylamine), poly(lysine), and poly(arginine) in polycation/RNA coacervates. Differences in RNA diffusion rates between PDAC/RNA and oligoarginine/RNA coacervates imply distinct biophysical environments. Template-directed RNA polymerization is relatively insensitive to Mg2+ concentration when performed in PDAC/RNA coacervates as compared to buffer, even enabling partial rescue of the reaction in the absence of magnesium. Finally, we show enhanced activities of multiple nucleic acid enzymes including two ribozymes and a deoxyribozyme, underscoring the generality of this approach, in which functional nucleic acids like aptamers and ribozymes, and in some cases key cosolutes localize within the coacervate microenvironments.
Highlights
Membraneless compartments, such as complex coacervates, have been hypothesized as plausible prebiotic micro-compartments due to their ability to sequester RNA; their compatibility with essential RNA World chemistries is unclear
We carried out template-directed primer extension reactions at pH 8.0 in the presence of different polyamines (Fig. 1b) that are largely protonated at this pH
Ribozyme-catalyzed RNA polymerization has been reported to be enhanced in the presence of 10-mer oligolysine and other heteropeptides derived from the ribosomal core proteins[31]; we did not observe any significant enhancement or inhibition of template-directed polymerization of RNA in the presence of a 10-mer oligolysine (K10), which has a charge density of 6.3 charge/kDa
Summary
Membraneless compartments, such as complex coacervates, have been hypothesized as plausible prebiotic micro-compartments due to their ability to sequester RNA; their compatibility with essential RNA World chemistries is unclear. Complex coacervates, which arise from phase separation of oppositely charged polyions, have been hypothesized as model protocells, or alternate biophysical compartments for prebiotic reactions[15,20,21] Membraneless compartments such as the nucleolus and RNP granules exist in modern cells and have their own biological functions[22,23,24]. The highly charged nature of RNA suggests that it could have participated in formation of complex coacervates with polycations on early-Earth, providing primitive compartments for functional RNAs such as ribozymes and RNA aptamers. Polycations such as polyamines have been shown to condense nucleic acids and form complex coacervates with nucleotides, RNA, and other anionic polymers[18,26,27]. The hammerhead ribozyme has recently been shown to retain some activity inside polylysine/
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