Coordinated wound responses in a regenerative animal-algal holobiont

Dania Nanes Sarfati, Yuan Xue, Eun Sun Song, Ashley Byrne, Daniel Le, Spyros Darmanis, Stephen R. Quake, Adrien Burlacot, James Sikes () and Bo Wang ()
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Dania Nanes Sarfati: Stanford University
Yuan Xue: Stanford University
Eun Sun Song: Stanford University
Ashley Byrne: Chan Zuckerberg Biohub
Daniel Le: Chan Zuckerberg Biohub
Spyros Darmanis: Chan Zuckerberg Biohub
Stephen R. Quake: Stanford University
Adrien Burlacot: Stanford University
James Sikes: University of San Francisco
Bo Wang: Stanford University

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Animal regeneration involves coordinated responses across cell types throughout the animal body. In endosymbiotic animals, whether and how symbionts react to host injury and how cellular responses are integrated across species remain unexplored. Here, we study the acoel Convolutriloba longifissura, which hosts symbiotic Tetraselmis sp. green algae and can regenerate entire bodies from tissue fragments. We show that animal injury causes a decline in the photosynthetic efficiency of the symbiotic algae, alongside two distinct, sequential waves of transcriptional responses in acoel and algal cells. The initial algal response is characterized by the upregulation of a cohort of photosynthesis-related genes, though photosynthesis is not necessary for regeneration. A conserved animal transcription factor, runt, is induced after injury and required for acoel regeneration. Knockdown of Cl-runt dampens transcriptional responses in both species and further reduces algal photosynthetic efficiency post-injury. Our results suggest that the holobiont functions as an integrated unit of biological organization by coordinating molecular networks across species through the runt-dependent animal regeneration program.

Date: 2024
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DOI: 10.1038/s41467-024-48366-2

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