Eukaryotes evade information storage-replication rate trade-off with endosymbiont assistance leading to larger genomes

Abstract: Genome length varies widely among organisms, from compact genomes of prokaryotes to vast and complex genomes of eukaryotes. In this study, we theoretically identify the evolutionary pressures that may have driven this divergence in genome length. We use a parameter-free model to study genome length evolution under selection pressure to minimize replication time and maximize information storage capacity. We show that prokaryotes tend to reduce genome length, constrained by a single replication origin, while eukaryotes expand their genomes by incorporating multiple replication origins. We propose a connection between genome length and cellular energetics, suggesting that endosymbiotic organelles, mitochondria and chloroplasts, evolutionarily regulate the number of replication origins, thereby influencing genome length in eukaryotes. We show that the above two selection pressures also lead to strict equalization of the number of purines and their corresponding base-pairing pyrimidines within a single DNA strand, known as Chagraff's second parity rule, a hitherto unexplained observation in genomes of nearly all known species. This arises from the symmetrization of replichore length, another observation that has been shown to hold across species, which our model reproduces. The model also reproduces other experimentally observed phenomena, such as a general preference for deletions over insertions, and elongation and high variance of genome lengths under reduced selection pressure for replication rate, termed the C-value paradox. We highlight the possibility of regulation of the firing of latent replication origins in response to cues from the extracellular environment leading to the regulation of cell cycle rates in multicellular eukaryotes.