Coordinated wound responses in a regenerative animal-algal photosymbiotic metaorganism

Animal regeneration requires coordinated responses of many cell types throughout the animal body. In animals carrying endosymbionts, cells from the other species may also participate in regeneration, but how cellular responses are integrated across species is yet to be unraveled. Here, we study the acoel Convolutriloba longifissura, which hosts symbiotic Tetraselmis green algae and can regenerate entire bodies from small tissue fragments. We show that animal injury leads to a decline in the photosynthetic efficiency of the symbiotic algae and concurrently induces upregulation of a cohort of photosynthesis-related genes. A deeply conserved animal transcription factor, runt, is induced after injury and required for the acoel regeneration. Knockdown of runt also dampens algal transcriptional responses to the host injury, particularly in photosynthesis related pathways, and results in further reduction of photosynthetic efficiency post-injury. Our results suggest that the runt-dependent animal regeneration program coordinates wound responses across the symbiotic partners and regulates photosynthetic carbon assimilation in this metaorganism. Overall design: In the first condition, Acoels were amputated, and their RNA were extracted at 0 or 3 hours post amputation. In the second condition, Acoels were treated with either control or Runt RNAi, amputated, and their RNA were extracted at different timepoints. In the third condition, we treated worms with low or high light exposure for varying duration before extracting their RNA. At least three replicates each containing five Acoel animals were used for RNA extraction for each condition.