Decoding a Multigenomic Symphony: Divergent Evolutionary Tempos Across the Four Genomic Compartments of Teleaulax Cryptophytes

Secondary endosymbiosis drives eukaryotic diversification by integrating genetic compartments from disparate lineages, yet how the host and endosymbiont genomes co-evolve over deep time remains poorly understood. Cryptophytes provide a compelling model to dissect this integration, as they uniquely retain four distinct genomes within a single cell: the host nucleus and mitochondrion, alongside a red algal-derived plastid and its relict nucleus (nucleomorph). Here, we investigate the evolutionary and regulatory dynamics of these four coexisting genomes in two ecologically important cryptophytes, Teleaulax amphioxeia and Teleaulax acuta. We reveal a striking decoupling of evolutionary tempos across these genomic compartments. Plastid genomes exhibit structural and functional stasis, while mitochondrial genomes, despite also maintaining high synteny, show faster sequence evolution and mobile element invasion. Nucleomorph genomes evolves even more rapidly, but their gene expression is rigid, with regulatory flexibility limited to a small, conserved set of plastid-supporting genes. Intriguingly, Teleaulax host nuclear genomes have undergone massive expansion, likely driven by ancient whole-genome duplication that might explain their greatest divergence among the four genomic compartments. This divergence is further characterised by differential expansion of gene families (e.g., PHYB-like photoreceptors and motor-related proteins) potentially linked to ecological adaptation. Diel transcriptomic analyses highlight conserved core metabolic responses across both species, but also unveil lineage-specific adaptations, such as enhanced circadian regulation in T. acuta associated with PHYB-like gene expansion. Overall, our findings uncover a constraint gradient from plastid stasis to high evolutionary flexibility toward nucleus, highlighting how secondary plastid-bearing cells achieve a balance between long-term stability and adaptive innovation.