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Overview of G. fascicularis and its two tentacle types. a The result of aggressive behavior between Galaxea fascicularis and Pavona sp. The yellow arrow shows the Galaxea, the white arrow shows the dead area between the two corals. Photo taken in Eilat by Tali Mass. b Catch tentacles (CT, green arrow) and extended sweeper tentacles (ST, black arrow) of G. fascicularis. c and i Overall histology of Alcian Blue-stained CT (c) and ST (i). Red boxes show the approximate location of high-magnification micrographs in this figure, blue squares show approximate location of micrographs in Fig. 2. d-f Histological sections of the tip of the CT, stained with H&E (upper section in d and panel e) and with Alcian Blue (lower section in d and panel f). e and f are magnifications of the orange square in (d). Note the tightly-packed large nematocytes in the ectoderm (ec, sp - spirocysts, MpM - Microbasic p Mastigophores) and the abundance of symbiotic algae (zo) in the endoderm (en). g, h Main types of nematocytes of the acrosphere (Microbasic p Mastigophores, MpMs, which have a smooth shaft, unlike the barbed shaft of the MbMs of the sweeper tentacles). i-l Histological sections of the tip of the ST, stained with H&E (upper section in j and panel k) and with Alcian Blue (lower section in j and panel l). k and l are magnifications of the yellow square in (j). Note the mucocytes in the ectoderm between the large, elongated nematocytes, and the lack of symbionts in the endoderm. Mucocytes (mc), mucus vesicles (mv) and nematocysts are stained in blue, the latter perhaps due to the presence of poly-gamma-glutamate (an acidic polyanion) in the capsule matrix of the nematocysts. Hi-Holotrichous isorhiza nematocytes. m, n Main types of nematocytes of the acrosphere of the ST (Microbasic b Mastogophores, MbMs). Scale bars are 100 μm for (c and i), 50 μm for (d and j), 200 μm for (e, f, k and l), 25 μm for (g, m) and 10 μm for (h, n)
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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...
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Stony corals (Scleractinia) are in the Phylum Cnidaria (cnidae referring to various types of stinging cells). They may be solitary or colonial, but all secrete an external, supporting aragonite skeleton. Large, colonial members of this phylum are responsible for the accretion of coral reefs in tropical and subtropical waters that form the foundatio...
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... Corals can also feed heterotrophically, by actively preying on dissolved (DOM) and particulate organic matter (POM) of varying size classes (Houlbrèque & Ferrier-Pagès, 2009), to obtain nutrients such as nitrogen and phosphorus that support both the coral host and if present, the Symbiodiniaceae (Fitt & Cook, 2001;Muscatine & Porter, 1977). The heterotrophic uptake of POM is facilitated by morphological adaptations such as feeding tentacles, mesenterial filaments, cnidae and even mucus, to effectively capture prey from the water column (Al-Sofyani & Niaz, 2007;Yosef et al., 2020). The extent to which corals rely on autotrophy and heterotrophy not only varies considerably between species but is also modulated by the environment (Palardy et al., 2008). ...
Coral energy and nutrient acquisition strategies are complex and sensitive to environmental conditions such as water flow. While high water flow can enhance feeding in hard corals, knowledge about the effects of water flow on the feeding of soft corals, particularly those pulsating, is still limited. In this study, we thus investigated the effects of feeding and water flow on the physiology of the pulsating soft coral Xenia umbellata. We crossed three feeding treatments: (i) no feeding, (ii) particulate organic matter (POM) in the form of phytoplankton and (iii) dissolved organic carbon (DOC) in the form of glucose, with four water volume exchange rates (200, 350, 500 and 650 L h −1) over 15 days. Various ecophysiological parameters were assessed including pulsation rate, growth rate, isotopic and elemental ratios of carbon (C) and nitrogen (N) as well as photo-physiological parameters of the Symbiodiniaceae (cell density, chlorophyll-a and mitotic index). Water flow had no significant effect but feeding had a substantial impact on the physiology of the X. umbellata holobiont. In the absence of food, corals exhibited significantly lower pulsation rates, lower Symbiodiniaceae cell density and lower mitotic indices compared to the fed treatments, yet significantly higher chlorophyll-a per cell and total N content. Differences were also observed between the two feeding treatments, with significantly higher pulsation rates and lower chlorophyll-a per cell in the DOC treatment, but higher C and N content in the POM treatment. Our findings suggest that the X. umbellata holobiont can be viable under different trophic strategies, though favouring mixotrophy. Additionally, the physiology of the X. umbellata may be regulated through its own pulsating behaviour without any positive or negative effects from different water flow. Therefore, this study contributes to our understanding of soft coral ecology, particularly regarding the competitive success and widespread distribution of X. umbellata. K E Y W O R D S carbon, current regime, nitrogen, phytoplankton, trophic ecology
... Corals in the ocean actively compete for space through sweeper tentacles. [13] Inspired by this conception of sweeper tentacles, we proposed an active self-cleaning surface with filament-like sweepers (Figure 1c). By utilizing energy from outer turbulent flows, the sweepers can penetrate the viscous sublayer and remove contaminants with adhesion stress of >30 kPa. ...
Hydrodynamic forces from moving fluids can be utilized to remove contaminants which is an ideal fouling‐release strategy for underwater surfaces. However, the hydrodynamic forces in the viscous sublayer are greatly reduced owing to the no‐slip condition, which restricts their practical applications. Here, inspired by sweeper tentacles of corals, an active self‐cleaning surface with flexible filament‐like sweepers are reported. The sweepers can penetrate the viscous sublayer by utilizing energy from outer turbulent flows and remove contaminants with adhesion strength of >30 kPa. Under an oscillating flow, the removal rate of the single sweeper can reach up to 99.5% due to dynamic buckling movements. In addition, the sweepers array can completely clean its coverage area within 10 s through coordinated movements as symplectic waves. The active self‐cleaning surface depends on the fluid‐structure coupling between sweepers and flows, which breaks the concept of conventional self‐cleaning.
... Coral larvae are known to prefer red over white surfaces for settling [22]. Corals can fight, so they must be able to sense and attack the enemy or competitor [23]. Corals can distinguish organisms to tolerate (symbiosis) versus subjecting them to an immune attack to prevent disease [24]. ...
With the ease of gene sequencing and the technology available to study and manipulate non-model organisms, the extension of the methodological toolbox required to translate our understanding of model organisms to non-model organisms has become an urgent problem. For example, mining of large coral and their symbiont sequence data is a challenge, but also provides an opportunity for understanding functionality and evolution of these and other non-model organisms. Much more information than for any other eukaryotic species is available for humans, especially related to signal transduction and diseases. However, the coral cnidarian host and human have diverged over 700 million years ago and homologies between proteins in the two species are therefore often in the gray zone, or at least often undetectable with traditional BLAST searches. We introduce a two-stage approach to identifying putative coral homologues of human proteins. First, through remote homology detection using Hidden Markov Models, we identify candidate human homologues in the cnidarian genome. However, for many proteins, the human genome alone contains multiple family members with similar or even more divergence in sequence. In the second stage, therefore, we filter the remote homology results based on the functional and structural plausibility of each coral candidate, shortlisting the coral proteins likely to have conserved some of the functions of the human proteins. We demonstrate our approach with a pipeline for mapping membrane receptors in humans to membrane receptors in corals, with specific focus on the stony coral, P. damicornis. More than 1000 human membrane receptors mapped to 335 coral receptors, including 151 G protein coupled receptors (GPCRs). To validate specific sub-families, we chose opsin proteins, representative GPCRs that confer light sensitivity, and Toll-like receptors, representative non-GPCRs, which function in the immune response, and their ability to communicate with microorganisms. Through detailed structure-function analysis of their ligand-binding pockets and downstream signaling cascades, we selected those candidate remote homologues likely to carry out related functions in the corals. This pipeline may prove generally useful for other non-model organisms, such as to support the growing field of synthetic biology.
... A close examination of the tentacles in Figure 6 (seen also in Figures 1B, 2D) shows that they contain batteries of stinging cells along the tentacles, and in particular, a knob-like structure at the tentacles' tip, called acrosphere. These acrospheres are characterized by a dense layer of nematocytes (Acuña and Garese, 2009;Yosef et al., 2020), exactly where the hydrodynamic mixing is the highest (see set E2 in Figure 5A and sets E11 and E15 in Figure 5B). One may wonder if the increased number of nematocysts, exactly where mixing intensity is the highest, is adaptive for food capture. ...
Key biological processes that are related to feeding, growth, and mortality in corals and other benthic organisms, depend on the flow field around them. For example, in the absence of flow, oxygen is accumulated inside and around photoautotrophic organisms such as algae and corals, and the rate of photosynthesis is therefore reduced. When mixing by turbulence and by streamline separation is suppressed, nutrient supply is reduced and prey capture becomes insufficient. Despite the overwhelming ecological impacts of flow on corals, almost no in-situ studies focused on the hydrodynamics at the scale of the coral polyps and their tentacles. Here we report on in-situ measurements obtained by an underwater Particle Image Velocimetry (PIV) above the tentacles of the massive coral Dipsastraea favus. The tentacles in this species, approximately 5-10 mm long, extend during the night and contract during the day. A comparison was made between the flow field around the coral when the tentacles were contracted and extended. As in large-scale canopy flows such as forests or urban areas, we found that when the tentacles were extended, a mixing layer rather than a boundary layer was formed above the coral. Velocities in between the tentacles were reduced, resident time increased, and velocity instabilities developed around the tentacle tips. Our in-situ measurements under the conditions of contracted tentacles agreed well with laboratory measurements obtained above dead skeletons of D. favus. When the tentacles were extended, a velocity profile typical for canopy flows developed, having a clear inflection point near the interface between the tentacles and the layer of free flow. The relative velocity fluctuations increased up to 3.5-fold compared with the state of contracted tentacles. The highest mixing was around the distal ends of the tentacles, where knob-like spheres named acrospheres contain extremely high concentrations of nematocytes. The intense mixing, the ensuing slowing down of prey movement, and its longer residence time within that zone may augment prey capture by the coral. These findings can explain the ubiquitous occurrence of acrospheres in benthic cnidarians.
... A range of ecological factors have been shown to impact on the venom profile and expenditure in cnidarians (O'Hara et al., 2021). Briefly, venom variations and/or changes have been attributed to differences in temperature (Jouiaei et al., 2015a;O'Hara et al., 2018;Oakley et al., 2017;Richier et al., 2008;Sachkova et al., 2020;Sunagawa et al., 2009), age (Columbus-Shenkar et al., 2018Klompen et al., 2018;McClounan and Seymour, 2012;Underwood and Seymour, 2007), diet (Underwood and Seymour, 2007), location (Winter et al., 2010;Yue et al., 2019), salinity (Sachkova et al., 2020), ultraviolet radiation (Richier et al., 2008;Sachkova et al., 2020), interspecies competition (Yosef et al., 2020) and predation pressure (Ben-Ari et al., 2018). ...
... Antagonistic encounters with competitors may also cause some anthozoans to develop specialized tentacles, such as, catch (Actiniaria), sweeper (Scleractinia) or bulbous (Corallimorpharia) tentacles (Langmead and Chadwick-Furman, 1999;Williams, 1991). This transformation includes significant alterations to the cnidom (Langmead and Chadwick-Furman, 1999;Miles, 1991), and venom toxicity (Yosef et al., 2020). Additionally, once the perceived threat has subsided, the animals may revert their tentacles back to their original feeding tentacle state (Williams, 1991). ...
Cnidarian bleaching research often focuses on the effects on a cnidarian's physiological health and fitness, whilst little focus has been towards the impacts of these events on their venom ecology. Given the importance of a cnidarian's venom to their survival and the increasing threat of bleaching events, it is important to understand the effects that this threat may have on this important aspect of their ecology as it may have unforeseen impacts on their ability to catch prey and defend themselves. This review aims to explore evidence that suggests that bleaching may impact on each of the key aspects of a cnidarians' venom ecology: cnidae, venom composition, and venom toxicity. Additionally, the resulting energy deficit, compensatory heterotrophic feeding, and increased defensive measures have been highlighted as possible ecological factors driving these changes. Suggestions are also made to guide the success of research in this field into the future, specifically in regards to selecting a study organism, the importance of accurate symbiont and cnidae identification, use of appropriate bleaching methods, determination of bleaching, and animal handling. Ultimately, this review highlights a significant and important gap in our knowledge into how cnidarians are, and will, continue to be impacted by bleaching stress.
... Coral larvae are known to prefer red over white surfaces for settling (Mason et al., 2011). Corals can fight, so they must be able to sense and attack the enemy or competitor (Yosef et al., 2020). Corals can distinguish organisms to tolerate (symbiosis) versus subjecting them to an immune attack to prevent disease (Mansfield & Gilmore, 2019). ...
With the ease of gene sequencing and the technology available to study and manipulate non-model organisms, the need to translate our understanding of model organisms to non-model organisms has become an urgent problem. For example, mining of large coral and their symbiont sequence data is a challenge, but also provides an opportunity for understanding functionality and evolution of these and other non-model organisms. Much more information than for any other eukaryotic species is available for humans, especially related to signal transduction and diseases. However, the coral cnidarian host and human have diverged over 700 million years ago and homologies between proteins are therefore often in the gray zone or undetectable with traditional BLAST searches. We introduce a two-stage approach to identifying putative coral homologues of human proteins. First, through remote homology detection using Hidden Markov Models, we identify candidate human homologues in the cnidarian genome. However, for many proteins, the human genome alone contains multiple family members with similar or even more divergence in sequence. In the second stage, therefore, we filter the remote homology results based on the functional and structural plausibility of each coral candidate, shortlisting the coral proteins likely to be true human homologues. We demonstrate our approach with a pipeline for mapping membrane receptors in humans to membrane receptors in corals, with specific focus on the stony coral, P. damicornis. More than 1000 human membrane receptors mapped to 335 coral receptors, including 151 G protein coupled receptors (GPCRs). To validate specific sub-families, we chose opsin proteins, representative GPCRs that confer light sensitivity, and Toll-like receptors, representative non-GPCRs, which function in the immune response, and their ability to communicate with microorganisms. Through detailed structure-function analysis of their ligand-binding pockets and downstream signaling cascades, we selected those candidate remote homologues likely to carry out related functions in the corals. This pipeline may prove generally useful for other non-model organisms, such as to support the growing field of synthetic biology.
... 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. ...
... 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). ...
Phylum Cnidaria is an ancient venomous group defined by the presence of cnidae, specialised organelles that serve as venom delivery systems. The distribution of cnidae across the body plan is linked to regionalisation of venom production, with tissue-specific venom composition observed in multiple actiniarian species. In this study, we assess whether morphological variants of tentacles are associated with distinct toxin expression profiles and investigate the functional significance of specialised tentacular structures. Using five sea anemone species, we analysed differential expression of toxin-like transcripts and found that expression levels differ significantly across tentacular structures when substantial morphological variation is present. Therefore, the differential expression of toxin genes is associated with morphological variation of tentacular structures in a tissue-specific manner. Furthermore, the unique toxin profile of spherical tentacular structures in families Aliciidae and Thalassianthidae indicate that vesicles and nematospheres may function to protect branched structures that host a large number of photosynthetic symbionts. Thus, hosting zooxanthellae may account for the tentacle-specific toxin expression profiles observed in the current study. Overall, specialised tentacular structures serve unique ecological roles and, in order to fulfil their functions, they possess distinct venom cocktails.
... Putative toxin genes were identified using reciprocal best-BLAST hits as described in Rachamim et al. (2015) and Yosef et al. (2020). 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). ...
Polyps in different locations on individual stony coral colonies experience variation in numerous environmental conditions including flow and light, potentially leading to transcriptional and physiological differences across the colony. Here, we describe high-resolution tissue and skeleton measurements and differential gene expression from multiple locations within a single colony of Stylophora pistillata, aiming to relate these to environmental gradients across the coral colony. We observed broad transcriptional responses in both the host and photosymbiont in response to height above the substrate, cardinal direction, and, most strongly, location along the branch axis. Specifically, several key physiological processes in the host appear more active toward branch tips including several metabolic pathways, toxin production for prey capture or defense, and biomolecular mechanisms of biomineralization. Further, the increase in gene expression related to these processes toward branch tips is conserved between S. pistillata and Acropora spp. The photosymbiont appears to respond transcriptionally to relative light intensity along the branch and due to cardinal direction. These differential responses were observed across the colony despite its genetic homogeneity and likely inter-polyp communication. While not a classical division of labor, each part of the colony appears to have distinct functional roles related to polyps’ differential exposure to environmental conditions.
... 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 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. ...
... 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 Positive ranks represent transcripts up-regulated in competition compared to controls. ...
Competitive interactions shape coral assemblages and govern the dynamics of coral ecosystems. Although competition is an ecological concept, the outcomes of competitive interactions are ultimately determined by patterns of gene expression. These patterns are subject to genotypic variation on both sides of any interaction. Such variation is typically treated as “noise”, but it is sometimes possible to identify patterns within it that reveal important hidden factors in an experiment. To incorporate genotypic variation into the investigation of coral competitive interactions, we used RNA-sequencing to study changes in gene expression in a hard coral (Porites cylindrica) resulting from non-contact competition experiment with a soft coral (Lobophytum pauciflorum). Hard coral genotype explained the largest proportion of variation between samples; however, it was also possible to detect gene expression changes in 76 transcripts resulting from interaction with the soft coral. In addition, we found a group of 20 short secreted proteins that were expressed as a coordinated unit in three interacting Porites-Lobophytum pairs. The presence of this secretion response was idiosyncratic in that it could not be predicted based on polyp behaviour, or the genotype of hard or soft coral alone. This study illustrates the significance of individual variation as a determinant of competitive behaviour, and also provides some intriguing glimpses into the molecular mechanisms employed by hard corals competing at a distance.
