Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution

PLoS Genet. 2023 Aug 4;19(8):e1010471. doi: 10.1371/journal.pgen.1010471. eCollection 2023 Aug.

Abstract

The integration of individually replicating genes into a primitive chromosome is a key evolutionary transition in the development of life, allowing the simultaneous inheritance of genes. However, how this transition occurred is unclear because the extended size of primitive chromosomes replicate slower than unlinked genes. Theoretical studies have suggested that a primitive chromosome can evolve in the presence of cell-like compartments, as the physical linkage prevents the stochastic loss of essential genes upon division, but experimental support for this is lacking. Here, we demonstrate the evolution of a chromosome-like RNA from two cooperative RNA replicators encoding replication and metabolic enzymes. Through their long-term replication in cell-like compartments, linked RNAs emerged with the two cooperative RNAs connected end-to-end. The linked RNAs had different mutation patterns than the two unlinked RNAs, suggesting that they were maintained as partially distinct lineages in the population. Our results provide experimental evidence supporting the plausibility of the evolution of a primitive chromosome from unlinked gene fragments, an important step in the emergence of complex biological systems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chromosomes*
  • Evolution, Molecular
  • Mutation
  • RNA* / genetics

Substances

  • RNA

Grants and funding

This work was supported by Japan Society for the Promotion of Science KAKENHI (21H05867 and 23H04403 to R.M., 22H05402 to N.I.) and Japan Science and Technology Agency PRESTO (JPMJPR19KA to R.M.) and CREST (JPMJCR20S1 to N.I.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.