A predatory gastrula leads to symbiosis-independent settlement inAiptasia

Abstract

The planulae larvae of cnidarians (jellyfish, hydras, anemones, corals) have attracted interest since Haeckels 150-year-old postulation of the gastrula developmental stage of sponges and corals as the terminal lifeform of primitive multicellular metazoans. Widely viewed as primarily particle feeders, the planulae larvae of the anemone Exaiptasia pallida (commonly Aiptasia) have not been reported to undergo settlement and metamorphosis to adult morphology, and the lack of a closed lifecycle has been a major obstacle in this increasingly popular model system for coral-dinoflagellate endosymbiosis. Here we studied Aiptasia larvae feeding behavior and show its indispensability to trigger the first reports of settlement and metamorphosis in the system, finally closing the Aiptasia lifecycle. Surprisingly, the young gastrula-like planulae at just two days post fertilization actively feed on living crustacean nauplii, preferentially to heat-killed ones. Predation is dependent on functional stinging cells (nematocytes), indicative of complex neuronal control. Larvae fed daily dramatically increase in size and at 14 days post fertilization begin to morphologically change prior to settlement at high efficiency. Strikingly, dinoflagellate endosymbionts are neither required for larval growth nor measurably affect settlement dynamics, but are essential for spawning of the mature adult polyps. Our data show for the first time that gastrula-like planulae were capable of prey capture, suggesting carnivory in addition to filter feeding as a common strategy of this terminal life form. These data are discussed in the context of recent revelations on the evolution of basal metazoans.

Editorial: Aiptasia: a model system in coral symbiosis research

“…Aiptasia has been adopted by a growing number of laboratories to explore research questions on: development and cellular regeneration (Fransolet et al, 2012;Fransolet et al, 2013;Bucher et al, the onset, maintenance, and disruption of symbiosis (Bieri et al, 2016;Bucher et al, 2016;Wolfowicz et al, 2016;Tivey et al, 2022;Rädecker et al, 2023); and metabolic interactions (Rädecker et al, 2018) among others. To date, this community of researchers has made available a genome (Baumgarten et al, 2015), developed omics tools (Lehnert et al, 2014;Baumgarten et al, 2018;Matthews et al, 2018;Simona et al, 2019;Sproles et al, 2019), closed the life cycle (Maegele et al, 2023), and openly shared their research protocols through initiatives such as the "Aiptasia Symbiosis Resource" portal (aiptasia-resource.org). But to make this sea anemone a practical and reliable model system in coral reef research and the symbiosis field more widely, the Aiptasia community still needs to overcome a few hurdles such as developing gene-editing tools, new imaging techniques, etc.…”