Endosymbiotic algal photosynthesis shapes diel transcriptome architecture in its ciliate host Paramecium bursaria

Abstract

How photosynthetic endosymbionts reorganize host daily regulation remains unclear. Paramecium bursaria displays pronounced day-night behaviors, but whether its algal symbionts drive host temporal programs has been unresolved. We compared host gene expressions across a 24-hour light-dark cycle in symbiotic and aposymbiotic cells. Symbiotic cells exhibit an expanded and highly temporally ordered diel transcriptome compared with aposymbiotic cells. These rhythmic programs encompass motility, signaling, metabolism, and growth regulation, consistent with observed behaviors. Symbiosis-associated rhythmic programs recruit gene families encoding post-translational regulatory domains, including kinases, ubiquitin-related factors, WD40 scaffolds, and calcium-binding proteins, despite lacking recognizable canonical clock genes. Disrupting photosynthesis with paraquat altered these temporal profiles, shifting them toward an aposymbiotic-like state. A distantly related ciliate, Tetrahymena utriculariae, with an independently evolved symbiosis, showed similar symbiosis-associated daily programs, suggesting that photosynthetic endosymbionts can act as important organizers of host daily gene regulation in endosymbiotic protists.