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 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 neurotoxic and hemolytic activities, consistent with a role in prey capture, whereas the STs have higher phospholipase A2 activity, which we speculate may have a role in inducing tissue damage during territorial aggression. The toxin genes expressed in each tentacle are also different. 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.

Physiological and transcriptomic variability indicative of differences in key functions within a single coral colony

“…Putative toxin genes were identified using reciprocal best-BLAST hits as described in (Rachamim et al, 2015;Yosef et al, 2020) (Supplementary Table 14). Differential expression of genes coding for known biomineralization-related proteins from S. pistillata skeleton or the calicoblastic layer were examined (Puverel et al, 2005;Drake et al, 2013;Mass et al, 2013;Zoccola et al, 2015;Peled et al, 2020) (Supplementary Table 16).…”

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

“…For example, the assassin bug Pristhesancus plagipennis and the cone snail Conus geographus produce distinct venoms specialised for predation and defence [ 46 , 47 ]. Differences in toxin expression across sweeper and feeding tentacles in corals can likewise be explained by the discrete roles of these two structures in intraspecific combat and prey capture, respectively [ 24 ]. While ecological interactions have minimal impact on the toxin gene complement in cnidarian species, they are known to function as keys drivers of toxin gene expression [ 14 , 25 , 48 , 49 ].…”

“…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.…”

Transcriptional responses indicate acclimation to prolonged deoxygenation in the coral Stylophora pistillata

“…Indeed, a s i g n ifi c an t d ow n -r e g u l a t i on o f t h e e x p r e s s i o n o f nematogalactin and minicollagen-1, essential for nematocyst formation (Beckmann and Özbek, 2012) is observed at one week, and becomes more prominent over time (Figure 6B (7), ( 8)), supporting down-regulation of nematocyst formation. Nematocysts are essential for predation, defense and for territorial aggression (Yosef et al, 2020), therefore these results could indicate that prolonged deoxygenation enhance the corals' dependence on symbiosis-derived components and reduce its predation efforts.…”