Pathways of early evolution from the perspectives of a riboreplisome -- the ultimate RNA machine of life

Abstract

Translation of the genetic code into proteins is universal across life, with ribosomes serving as the ancient molecular machines enabling this information transformation. We propose that early replication and protein biosynthesis were inseparable functions performed by a single ancient RNA molecule: the riboreplisome. This hypothesis addresses fundamental challenges facing RNA world, protein world, and RNA-protein co-evolution theories -- particularly the problem of non-Darwinian starting points and the interdependence of replication and translation machineries. We present a 12-step evolutionary pathway from simple RNA replicase to proto-ribosome, supported by quantitative modelling demonstrating that only two steps require non-Darwinian transitions while the remaining ten proceed through standard selection. The single-molecule riboreplisome architecture provides an approximately 6-fold evolutionary advantage over multi-component "RNA soup" scenarios, principally by maintaining genetic linkage and retaining catalytic products close to the replicating genome (resisting diffusion loss); structural resistance to parasitic "cheater" molecules follows as a corollary. The riboreplisome framework explains the origins of ribosomal, transfer, and messenger RNA as derivatives of a single ancestral molecule, while providing a driving force for cellular compartmentalisation. Although the original riboreplisome is likely lost to deep time, molecular remnants may persist in extant biological RNA. Identification or reconstruction of riboreplisome-like molecules could advance both origin-of-life research and synthetic biology applications.