How to upgrade stolen organelles into permanent plastids: A comparative transcriptomic perspective.

Abstract

Tertiary plastids derived from diatoms in "dinotom" dinoflagellates offer a rare view of organellogenesis in action, while the genomic and metabolic processes underlying their conversion remain poorly understood. Here, we present a comparative transcriptomic analysis of two dinotoms at different plastidial levels: <i>Durinskia capensis</i> at the kleptoplastidy state, alongside its kleptoplastid-source diatom <i>Nitzschia captiva</i>, and its close relative <i>Durinskia kwazulunatalensis</i> at an early permanent state. We show that in both dinotoms, the diatom nucleus retains high transcriptional autonomy, but its expression profile is plastid biased, signaling early host influence. In contrast, only <i>D. kwazulunatalensis</i> exhibits striking signs of genomic reconfiguration in the diatom nucleus: intron insertions, increased guanine (G) and cytosine (C) content, and growing nucleotide similarity to host transcripts. These shifts suggest an incipient nucleomorph-like transformation. Metabolically, only <i>D. kwazulunatalensis</i> expresses a complete hexose phosphate export pathway, suggesting deeper metabolic integration, while both species retain simpler carbohydrate transport routes. Additionally, we propose that diatom karyokinesis might be controlled by a dual mechanism via suppression of key transcription factors at the G1-S checkpoint and nitrate availability. Together, our findings reveal a continuum of plastid integration degrees, from temporary organelle theft to genomic accommodation and metabolic codependence. Dinotoms thus serve not only as evolutionary artifacts but as living laboratories, illuminating how kleptoplastids inch toward permanence.