Co-option of lysosomal machinery shapes the symbiosis supporting coral reefs

Abstract

Intracellular photosymbiosis has evolved across life and forms the foundation of coral reef ecosystems. Using the sea anemone Aiptasia as a model, we generated a high-quality proteome of the symbiosome, the organelle that houses algal symbionts. This proteome revealed protein trafficking mechanisms and the types of biomolecules exchanged during symbiosis. Symbiosomal enrichment of lysosomal proteins, visualization of lysosomal fusion, along with reduced symbiosis following knockdown of lysosomal genes, supports its phagolysosomal identity and that extensive co-option of lysosomal proteins shapes the symbiosome. CRISPR/Cas9-induced mutations in the symbiosomal and lysosomal bicarbonate/sulfate transporter, SLC26A11, disrupted symbiosis in both Aiptasia and a reef-building coral. These findings support that anemones and corals independently evolved a carbon-concentrating and sulfate transport mechanism to fuel photosymbiosis by co-opting an orthologous lysosomal transporter.