Replication Rate-Information Storage Trade-Off Shapes Genome Architecture Across Domains.

Genome size varies widely among organisms, from compact genomes of bacteria to vast and complex genomes of eukaryotes. In this study, we theoretically investigate the evolutionary pressures that may have driven this divergence in genome size. We introduce a model, informed by DNA replication dynamics, to study genome size evolution under selection pressure to minimize replication time and maximize information storage capacity. We substantiate this choice by demonstrating a correlation between replication time and genome size using literature data. We show that bacteria tend to reduce genome size, constrained by a single replication origin, while eukaryotes expand their genomes by incorporating multiple replication origins. We argue that nucleotide skews, present in nearly all genomes studied, and are used to identify replication origins, directly influence DNA unzipping kinetics, and hence their replication time. This connection enables us to reproduce nearly universal observations, such as Chargaff’s second parity rule and replichore symmetrization, as adaptive consequences. We argue that high skews lead to faster replication, and substantiate it by showing a correlation between skews and replication speed in bacteria and archaea. The model reproduces more evolutionary genomic observations, such as a general preference for deletions over insertions across domains, and elongation and high variance of genome size under reduced selection pressure for replication rate, an integral component of the C-value paradox.