A tentacle for every occasion: comparing the hunting tentacles and sweeper tentacles, used for territorial competition, in the coral Galaxea fascicularis

Abstract

Background Coral reefs are among the most diverse, complex and densely populated marine ecosystems. To survive, morphologically simple and sessile cnidarians have developed mechanisms to catch prey, deter predators and compete with adjacent corals for space, yet the mechanisms underlying these functions are largely unknown. Here, we characterize the histology, toxic activity and gene expression patterns in two different types of tentacles from the scleractinian coral Galaxea fascilcularis – catch tentacles (CTs), used to catch prey and deter predators, and sweeper tentacles (STs), specialized tentacles used for territorial aggression. Results STs exhibit more mucocytes and higher expression of mucin genes than CTs, and lack the ectodermal cilia used to deliver food to the mouth and remove debris. STs and CTs also express different sensory rhodopsin-like g-protein coupled receptors, suggesting they may employ different sensory pathways. Each tentacle type has a different complement of stinging cells (nematocytes), and the expression in the two tentacles of genes encoding structural nematocyte proteins suggests the stinging cells develop within the tentacles. CTs have higher neurotoxicity to blowfly larvae and hemolytic activity compared to the STs, consistent with a role in prey capture. In contrast, STs have higher phospholipase A2 activity, which we speculate may have a role in inducing tissue damage during territorial aggression. The expression of genes encoding cytolytic toxins (actinoporins) and phospholipases also differs between the tentacle types. Conclusions These results show that the same organism utilizes two distinct tentacle types, each equipped with a different venom apparatus and toxin composition, for prey capture and defense and for territorial aggression.

The Significance of Genotypic Diversity in Coral Competitive Interaction: A Transcriptomic Perspective

“…Another working hypothesis is that these candidate toxins could reach the competitor through tentacle contact. Tentacle attack is usually seen through the development of sweeper tentacles where the tip is enriched in nematocyst and other toxins, as documented for Galaxea (Yosef et al, 2020) but this strategy has neither been registered for Porites nor was it observed in this experiment. Another possibility is that these proteins could be secreted into the surrounded water and reach a competitor via diffusion through the water column.…”

“…In addition, most field surveys and experiments to date have relied on visible signs to detect competitive interactions and determine their order of dominance. Visible competitive strategies of corals include: overtopping to starve competitors of light; deployment of mesenteric filaments to externally digest a competitor; and elongation of polyps or development of sweeper tentacles to enable contact followed nematocyst discharge [reviewed by Lang and Chornesky, 1990;Chadwick and Morrow, 2011;Yosef et al, 2020). Although these physical signs are reliable indicators of competition when competitors are in contact, it is now clear that a wide range of reef taxa including scleractinian corals, octocorals, sponges, and algae (Coll and Sammarco, 1983;Sammarco et al, 1983;Fearon and Cameron, 1996;Koh and Sweatman, 2000;Chadwick and Morrow, 2011) all produce toxins that could mediate competitive interactions without close contact.…”

Tentacle Morphological Variation Coincides with Differential Expression of Toxins in Sea Anemones

“…More toxin-like transcripts were differentially expressed between endocoelic tentacles and nematospheres (15) than between endocoelic tentacles and exocoelic tentacles (13). Overall, the highest number of differentially expressed toxin-like transcripts was observed when comparing the body column and nematospheres (24), and the lowest when comparing exocoelic tentacles and nematospheres (1).…”

“…Both catch and sweeper tentacles are specialised for agonistic encounters with competitors, causing necrosis in other polyps, and are morphologically distinct from feeding tentacles [20,22,23]. A recent investigation of gene expression in sweeper and feeding tentacles in the stony coral Galaxea fasicularis revealed that toxin genes are differentially expressed across the two tentacle subsets [24] indicating that venom composition may vary across tentacle types when they fulfil distinct ecological functions. We surmised that toxin expression might similarly differ in a tentacle-specific manner in sea anemones, given that they also possess functionally distinct tentacle subsets.…”

“…Given that differences in the functional profiles of structures correlate to the differential expression of toxins in a tissue-specific manner [14,15,24], distinct tentacle-specific toxin expression patterns may be present across tentacle subtypes that serve different ecological functions. Furthermore, there is likely to be a functional basis for morphological variants of tentacles observed in Aliciidae and Thalassianthidae.…”