A diverse host thrombospondin-type-1 repeat protein repertoire promotes symbiont colonization during establishment of cnidarian-dinoflagellate symbiosis

Abstract

The mutualistic endosymbiosis between cnidarians and dinoflagellates is mediated by complex inter-partner signaling events, where the host cnidarian innate immune system plays a crucial role in recognition and regulation of symbionts. To date, little is known about the diversity of thrombospondin-type-1 repeat (TSR) domain proteins in basal metazoans or their potential role in regulation of cnidarian-dinoflagellate mutualisms. We reveal a large and diverse repertoire of TSR proteins in seven anthozoan species, and show that in the model sea anemone Aiptasia pallida the TSR domain promotes colonization of the host by the symbiotic dinoflagellate Symbiodinium minutum . Blocking TSR domains led to decreased colonization success, while adding exogenous TSRs resulted in a ‘super colonization’. Furthermore, gene expression of TSR proteins was highest at early time-points during symbiosis establishment. Our work characterizes the diversity of cnidarian TSR proteins and provides evidence that these proteins play an important role in the establishment of cnidarian-dinoflagellate symbiosis. Cnidarians, such as corals and sea anemones, often form a close relationship with microscopic algae that live inside their cells – a partnership, on which the entire coral reef ecosystem depends. These microalgae produce sugars and other compounds that the cnidarians need to survive, while the cnidarians protect the microalgae from the environment and provide the raw materials they need to harness energy from sunlight. However, very little is known about how the two partners are able to communicate with each other to form this close relationship, which is referred to as a symbiosis.Symbiotic relationships between a host and a microbe require a number of adaptations on both sides, and involve numerous signalling molecules. A host species is under constant pressure to develop mechanisms to recognize and tolerate the beneficial microbes without leaving itself vulnerable to attack by microbes that might cause disease. Similarly, the beneficial microbes need to be able to invade and survive inside their host.Previous research has shown that TSR proteins in hosts play a role in recognizing and controlling disease-causing microbes. Until now, however, it was unknown whether TSR proteins are involved in establishing a symbiosis between cnidarians and their algal partners.Neubauer et al. analysed six species of symbiotic cnidarians and discovered a diverse repertoire of TSR proteins. These proteins were found in the host genomes, rather than in the symbiotic algae, strongly suggesting that they originated from the host.Neubauer et al. next incubated a sea anemone species in a solution of TSR proteins and saw that it became ‘super-colonized’ with algae, meaning that over time, millions of the microalgae entered and stayed in the anemone’s tentacles. In contrast, when the TSR proteins were blocked, colonization was almost entirely stopped. This suggests that host TSR proteins play an important role for the microalgae when they colonialize corals and other cnidarians.The signals that enable microalgae to successfully colonialize cnidarians are unquestionably complex and there is still much to learn. These findings add another piece to the puzzle of how symbiotic algae bypass the cnidarian’s immune system to persist and flourish in their host. An important next step will be to test how blocking the genes that encode the TSR proteins will affect the symbiotic relationship between these species.