Photosymbiotic algae acquisition and their interactions with the acoel Convolutriloba macropyga

Abstract

Symbiosis with photosynthetic microbes is widespread in marine animals, with various symbiont transmission modes and localisation within the host. Here, we characterise the association between the acoel Convolutriloba macropyga and its photosymbionts, identified as Tetraselmis green algae based on rbcL gene phylogenetic analysis. Symbionts are transmitted vertically to asexual offspring and acquired horizontally by juveniles after sexual reproduction. Embryos develop to aposymbiotic juveniles that ingest Tetraselmis through the mouth. Confocal microscopy shows an increase in algae number within juveniles and in their presence at the body wall. Transmission electron microscopy reveals that symbionts lose flagella and theca. In adults, symbionts are extracellular at the body periphery, but can be intracellular within the parenchyma, in contrast with previously described acoel photosymbionts. This likely reflects different host-symbiont interactions, with algae potentially performing photosynthesis and nutrient exchange at the periphery, while undergoing transport or digestion in the parenchyma. Comparative transcriptomics between symbiotic adults and aposymbiotic juveniles shows an enrichment of amino acid synthesis, lipid metabolism, and osmotic and oxidative stress responses in symbiotic adults. Our data shows that algal symbionts engage with host tissues in distinct ways, inside or outside host cells, highlighting a previously unappreciated spatial complexity in host-algae interactions. HighlightsO_LITetraselmis algae are taken up by Convolutriloba macropyga juveniles C_LIO_LIAlgal symbionts in juveniles lose theca and flagella, proliferate, and move to the body wall C_LIO_LISymbionts are extracellular at the body wall and can be intracellular in the parenchyma C_LIO_LIAmino acid synthesis, lipid metabolism, osmoregulation and stress responses are activated in symbiotic adults C_LI