A red algal polysaccharide influences the multicellular development of the choanoflagellate Salpingoeca rosetta

The choanoflagellate Salpingoeca rosetta exemplifies the capacity of marine microeukaryotes to integrate environmental cues into their life histories. Some of the cues that S. rosetta detects are lipids from their bacterial prey that induce the development of multicellular colonies called rosettes.^1,2,3 In the aquatic environments where S. rosetta would encounter bacterial cues, microbial communities gain refuge^{4,5,6,7,8,9,10,11} and food^12,13,14 from algae. For example, microbes in coastal environments benefit from macroalgae that annually release ∼10¹⁴ g of carbon,^15,16 primarily in the form of polysaccharides that comprise ∼80% of dissolved organic carbon in surface waters.¹⁷ Despite the ecological impact of algae and historical descriptions of choanoflagellates attached to algae,^18,19,20 the influence of algae on choanoflagellate life history transitions has remained unexplored. Here, we report that porphyran, a polysaccharide produced by the red macroalga Porphyra umbilicalis, induces multicellular development in S. rosetta. We first noticed this response when S. rosetta formed multicellular rosette colonies while growing in media prepared from P. umbilicalis, even though rosette-inducing bacteria were absent. By biochemically purifying extracts of P. umbilicalis, we identified porphyran as the rosette-inducing factor. This response provides a biochemical insight that indicates algal polysaccharides may serve as cues to mediate associations between choanoflagellates and algae. Moreover, this observation complements evidence from environmental and geochemical studies that show the impact that algae have exerted on the ecology and evolution of eukaryotes,²¹ including a rise in algal productivity during the origin of animals,²² the closest living relatives of choanoflagellates.