The Projectile Tooth of a Fish-Hunting Cone Snail:<i>Conus catus</i>Injects Venom Into Fish Prey Using a High-Speed Ballistic Mechanism

Schulz, Joseph R.; Norton, Alex G.; Gilly, William F.

doi:10.2307/1543581

Cited by 48 publications

(46 citation statements)

References 8 publications

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“…1 A and B) (3)(4)(5). When the tip of the proboscis comes in contact with the target, the radula is rapidly propelled into the prey and acts like a hypodermic needle to inject the venom (6). This radula tooth then serves as a harpoon to bring the captured prey back to the mouth of the snail (Fig.…”

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confidence: 99%

Optimized deep-targeted proteotranscriptomic profiling reveals unexplored Conus toxin diversity and novel cysteine frameworks

Lavergne

Harliwong

Jones

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Cone snails are predatory marine gastropods characterized by a sophisticated venom apparatus responsible for the biosynthesis and delivery of complex mixtures of cysteine-rich toxin peptides. These conotoxins fold into small highly structured frameworks, allowing them to potently and selectively interact with heterologous ion channels and receptors. Approximately 2,000 toxins from an estimated number of >70,000 bioactive peptides have been identified in the genus Conus to date. Here, we describe a high-resolution interrogation of the transcriptomes (available at www.ddbj.nig.ac.jp) and proteomes of the diverse compartments of the Conus episcopatus venom apparatus. Using biochemical and bioinformatic tools, we found the highest number of conopeptides yet discovered in a single Conus specimen, with 3,305 novel precursor toxin sequences classified into 9 known superfamilies (A, I1, I2, M, O1, O2, S, T, Z), and identified 16 new superfamilies showing unique signal peptide signatures. We were also able to depict the largest population of venom peptides containing the pharmacologically active C-C-CC-C-C inhibitor cystine knot and CC-C-C motifs (168 and 44 toxins, respectively), as well as 208 new conotoxins displaying odd numbers of cysteine residues derived from known conotoxin motifs. Importantly, six novel cysteine-rich frameworks were revealed which may have novel pharmacology. Finally, analyses of codon usage bias and RNA-editing processes of the conotoxin transcripts demonstrate a specific conservation of the cysteine skeleton at the nucleic acid level and provide new insights about the origin of sequence hypervariablity in mature toxin regions.

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confidence: 99%

Optimized deep-targeted proteotranscriptomic profiling reveals unexplored Conus toxin diversity and novel cysteine frameworks

Lavergne

Harliwong

Jones

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…At least one fish-hunting species, Conus catus, uses a high-speed hydraulic mechanism. During this process the highly specialized radular tooth is fired from its holding point near the tip of the proboscis into the prey in less than 1ms (Schulz et al, 2004). Prior to tooth ejection, a priming step occurs during which the radular tooth is forced against a constriction of the proboscis lumen.…”

Section: Introductionmentioning

confidence: 99%

“…Prior to tooth ejection, a priming step occurs during which the radular tooth is forced against a constriction of the proboscis lumen. This constriction was thought to be a muscular sphincter (Greene and Kohn, 1989) that contracts to retain the radular tooth prior to its release (Schulz et al, 2004). The energy needed to propel the tooth was hypothesized to be generated by an increase in pressure caused by sustained contraction of the proboscis' musculature, eventually sending the tooth past the constriction and into the prey (Schulz et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

“…This constriction was thought to be a muscular sphincter (Greene and Kohn, 1989) that contracts to retain the radular tooth prior to its release (Schulz et al, 2004). The energy needed to propel the tooth was hypothesized to be generated by an increase in pressure caused by sustained contraction of the proboscis' musculature, eventually sending the tooth past the constriction and into the prey (Schulz et al, 2004). Although the rapid motion of the radular tooth has been established, the mechanism responsible for generating this motion remains unclear.…”

Section: Introductionmentioning

confidence: 99%

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Venom kinematics during prey capture inConus: the biomechanics of a rapid injection system

Salisbury

Martin

Kier

et al. 2010

Journal of Experimental Biology

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high-speed video. Using light, fluorescence and transmission electron microscopy (TEM), we assessed the composition and function of specific tissues crucial for prey capture. Our integrative experimental approach offers a more comprehensive understanding of this well-developed mechanism in Conus.Kinematic studies of the mollusc-hunting C. pennaceus indicate that a high-speed prey capture mechanism is not unique to cone species that hunt fish prey capable of rapid escape responses. Conus pennaceus SUMMARY Cone snails use an extensile, tubular proboscis as a conduit to deliver a potent cocktail of bioactive venom peptides into their prey. Previous studies have focused mainly on understanding the venom's role in prey capture but successful prey capture requires both rapid physiological and biomechanical mechanisms. Conus catus, a fish-hunting species, uses a high-speed hydraulic mechanism to inject its hollow, spear-like radular tooth into prey. We take an integrated approach to investigating the biomechanics of this process by coupling kinematic studies with morphological analyses. Taking advantage of the opaque venom and translucent proboscis of a mollusc-hunting juvenile cone snail, Conus pennaceus, we have determined that a high-speed prey capture mechanism is not unique to cone species that hunt fish prey. Two morphological structures were found to play crucial roles in this process. A constriction of the lumen near the tip of the proboscis, composed of tall epithelial cells densely packed with microfilaments, impedes forward movement of the radular tooth prior to its propulsion. Proximal to the constriction, a muscular sphincter was found to regulate venom flow and pressurization in the proboscis. In C. pennaceus, the rapid appearance and flushing of venom within the proboscis during prey capture suggests a mechanism involving the delivery of a discrete quantity of venom. The interplay between these elements provides a unique and effective biomechanical injection system for the fast-acting cone snail venom peptides. Supplementary material available online at

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“…Mechanisms for transferring toxins from the venom duct into the proboscis for injection are not well understood, but in at least one species, C. californicus, peptides appear to be packaged into the radular teeth themselves (Marshall et al, 2002). In the fish-hunting species C. catus, and presumably in other species as well, the radular tooth is explosively propelled in a ballistic fashion into the prey prior to venom expulsion through the tooth (Schulz et al, 2004). Venoms of both C. striatus and C. catus induce an immediate tetanic paralysis of the harpooned fish, thereby enabling prey capture (Kohn, 1956).…”

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confidence: 99%

Intraspecific variation of venom injected by fish-hunting Conussnails

Jakubowski

Kelley

Sweedler

et al. 2005

Journal of Experimental Biology

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SUMMARY Venom peptides from two species of fish-hunting cone snails (Conus striatus and Conus catus) were characterized using microbore liquid chromatography coupled with matrix-assisted laser desorption/ionization-time of flight-mass spectrometry and electrospray ionization-ion trap-mass spectrometry. Both crude venom isolated from the venom duct and injected venom obtained by milking were studied. Based on analysis of injected venom samples from individual snails, significant intraspecific variation (i.e. between individuals) in the peptide complement is observed. The mixture of peptides in injected venom is simpler than that in the crude duct venom from the same snail, and the composition of crude venom is more consistent from snail to snail. While there is animal-to-animal variation in the peptides present in the injected venom, the composition of any individual's injected venom remains relatively constant over time in captivity. Most of the Conus striatus individuals tested injected predominantly a combination of two neuroexcitatory peptides (s4a and s4b),while a few individuals had unique injected-venom profiles consisting of a combination of peptides, including several previously characterized from the venom duct of this species. Seven novel peptides were also putatively identified based on matches of their empirically derived masses to those predicted by published cDNA sequences. Profiling injected venom of Conus catus individuals using matrix-assisted laser desorption/ionization-time of flight-mass spectrometry demonstrates that intraspecific variation in the mixture of peptides extends to other species of piscivorous cone snails. The results of this study imply that novel regulatory mechanisms exist to select specific venom peptides for injection into prey.

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The Projectile Tooth of a Fish-Hunting Cone Snail:Conus catusInjects Venom Into Fish Prey Using a High-Speed Ballistic Mechanism

Cited by 48 publications

References 8 publications

Optimized deep-targeted proteotranscriptomic profiling reveals unexplored Conus toxin diversity and novel cysteine frameworks

Optimized deep-targeted proteotranscriptomic profiling reveals unexplored Conus toxin diversity and novel cysteine frameworks

Venom kinematics during prey capture inConus: the biomechanics of a rapid injection system

Intraspecific variation of venom injected by fish-hunting Conussnails

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