RNA–DNA Chimeras in the Context of an RNA World Transition to an RNA/DNA World

Abstract

The RNA world hypothesis posits that DNA and proteins were later inventions of early life, or the chemistry that gave rise to life. Most scenarios put forth for the emergence of DNA assume a clean separation of RNA and DNA polymer, and a smooth transition between RNA and DNA. However, based on the reality of "clutter" and lack of sophisticated separation/discrimination mechanisms in a protobiological (and/or prebiological) world, heterogeneous RNA-DNA backbone containing chimeric sequences could have been common-and have not been fully considered in models transitioning from an RNA world to an RNA-DNA world. Herein we show that there is a significant decrease in Watson-Crick duplex stability of the heterogeneous backbone chimeric duplexes that would impede base-pair mediated interactions (and functions). These results point to the difficulties for the transition from one homogeneous system (RNA) to another (RNA/DNA) in an RNA world with a heterogeneous mixture of ribo- and deoxyribonucleotides and sequences, while suggesting an alternative scenario of prebiological accumulation and co-evolution of homogeneous systems (RNA and DNA).

Chimeric XNA: An Unconventional Design for Orthogonal Informational Systems

“…The observation that heterogeneous backbone duplexes containing alternating ribuloNA‐RNA or ribuloNA‐DNA residues are more stable than corresponding alternating RNA‐DNA duplexes is significant from two aspects: a) ribuloNA is a highly destabilizing alternative backbone system with no self‐pairing or RNA/DNA cross‐pairing capability, and, more importantly, b) chimeric‐backbone‐heterogeneous RNA–DNA duplexes are weaker than the corresponding homogeneous RNA or DNA duplexes, even though RNA and DNA cross‐pair efficiently with each other. The latter aspect is also true for many of the XNAs which base pair with complementary RNA and DNA with few exceptions .…”

“…By using the stronger ribulo-pyrimidine-ribo-purine ( r t-rA) combination, the "GC" unit can be impersonated,w hile the weaker ribulo-purine-ribo-pyrimidine r a-rT combinationsw ould simulatethe "AU" unit. The observation that heterogeneousb ackbone duplexes containing alternating ribuloNA-RNA or ribuloNA-DNA residues are more stable than corresponding alternating RNA-DNA duplexes is significant from two aspects:a )ribuloNA is ah ighly destabilizing alternative backbone system with no self-pairing or RNA/DNA cross-pairing capability, [17] and, more importantly, b) chimeric-backbone-heterogeneous RNA-DNA duplexes are weaker than the corresponding homogeneous RNA or DNA duplexes, [37] even thoughR NA and DNA cross-pair efficiently with each other.T he lattera specti sa lso true for many of the XNAs which base pair with complementary RNA and DNA [15] with few exceptions. [38] Considering these facts, the results presented here suggest an unusual design-thatcombining oligonucleotide systems which do not pairw ith themselves or cross-pair with others may lead to novel sequence-specific pairing systemsw ith more favorable functional profiles, while the opposite seems to occuru pon combining self-and crosspairing-capable systems.…”

The Landscape of the Emergence of Life

“…In the milieu of the prebiotic epoch, gradual chemical evolution of heterogeneous → homogeneous during the oligomeric/polymeric transitions led to the eventual emergence of homogeneous backbones of RNA:DNA → DNA/protein world as we recognise today. The net result being that it was a “chimeric oligonucleotide system” from which life emerged rather than a “pure” RNA world [49,50]. …”

Effects of Pressure and pH on the Hydrolysis of Cytosine: Implications for Nucleotide Stability around Deep‐Sea Black Smokers

“…[2] However,t hese scenarios are vigorously disputed in favour of protein-first FeS-templated origins. Through in situ NMR spectroscopy measurements, it has been determined that the half-life of cytosine at 373.15 Kd ecreases from (18.0 AE 0.7) days at ambient pressure (0.1 MPa) to (8.64 AE 0.18) days at high pressure (200 MPa).…”

“…[2] However,t hese scenarios are vigorously disputed in favour of protein-first FeS-templated origins. Many scenarios have RNA-based lifeforms preceding the extant protein-based life-forms, [1] or coevolution of RNA alongside DNA.…”