Cnidarian-Symbiodiniaceae symbiosis establishment is independent of photosynthesis

• Published in: Current biology 2022-06, Vol.32 (11), p.2402-2415.e4
• Main Authors: Jinkerson, Robert E., Russo, Joseph A., Newkirk, Casandra R., Kirk, Andrea L., Chi, Richard J., Martindale, Mark Q., Grossman, Arthur R., Hatta, Masayuki, Xiang, Tingting
• Format: Article
• Language: English
• Subjects: Acropora tenuis; Animals; Anthozoa; Cassiopea xamachana; Dinoflagellida; Exaiptasia pallida; infection; maintenance; Photosynthesis; proliferation; Sea Anemones; Symbiodiniaceae; Symbiosis; symbiosis establishment; UV mutagenesis
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2022.04.021

Photosynthesis shapes the symbiotic relationships between cnidarians and Symbiodiniaceae algae—with many cnidarian hosts requiring symbiont photosynthate for survival—but little is known about how photosynthesis impacts symbiosis establishment. Here, we show that during symbiosis establishment, infection, proliferation, and maintenance can proceed without photosynthesis, but the ability to do so is dependent on specific cnidarian-Symbiodiniaceae relationships. The evaluation of 31 pairs of symbiotic relationships (five species of Symbiodiniaceae in sea anemone, coral, and jellyfish hosts) revealed that infection can occur without photosynthesis. A UV mutagenesis method for Symbiodiniaceae was established and used to generate six photosynthetic mutants that can infect these hosts. Without photosynthesis, Symbiodiniaceae cannot proliferate in the sea anemone Aiptasia or jellyfish Cassiopea but can proliferate in the juvenile polyps of the coral Acropora. After 6 months of darkness, Breviolum minutum is maintained within Aiptasia, indicating that Symbiodiniaceae maintenance can be independent of photosynthesis. Manipulating photosynthesis provides insights into cnidarian-Symbiodiniaceae symbiosis. [Display omitted] •Cnidarian-Symbiodiniaceae symbiosis establishment can proceed without photosynthesis•Infection proceeds independent of photosynthesis in the 31 symbiotic pairs evaluated•Photosynthesis is required for proliferation in Aiptasia but not in Acropora polyps•Breviolum minutum photosynthetic mutants were created to investigate symbiosis Photosynthesis shapes the symbiotic relationships between cnidarian hosts and Symbiodiniaceae algae. Jinkerson et al. show that infection, proliferation, and maintenance can proceed without photosynthesis during symbiosis establishment, but the ability to do so depends on specific host-symbiont pairs.