scholarly journals Developmental modularity and phenotypic novelty within a biphasic life cycle: morphogenesis of a cone snail venom gland

2011 ◽  
Vol 279 (1726) ◽  
pp. 77-83 ◽  
Author(s):  
Louise R. Page
Keyword(s):  
Feeding Behaviour ◽  
Venom Gland ◽  
Cone Snail ◽  
Evolutionary Transition ◽  
Metamorphic Stage ◽  
Oesophageal Gland ◽  
Key Innovation ◽  
Biphasic Life Cycle ◽  
Epithelial Sheet ◽  
Phenotypic Novelty

The venom gland of predatory cone snails ( Conus spp.), which secretes neurotoxic peptides that rapidly immobilize prey, is a proposed key innovation for facilitating the extraordinary feeding behaviour of these gastropod molluscs. Nevertheless, the unusual morphology of this gland has generated controversy about its evolutionary origin and possible homologues in other gastropods. I cultured feeding larvae of Conus lividus and cut serial histological sections through the developing foregut during larval and metamorphic stages to examine the development of the venom gland. Results support the hypothesis of homology between the venom gland and the mid-oesophageal gland of other gastropods. They also suggest that the mid-region of the gastropod foregut, like the anterior region, is divisible into dorsal and ventral developmental modules that have different morphological, functional and ontogenetic fates. In larvae of C. lividus , the ventral module of the middle foregut transformed into the anatomically novel venom gland of the post-metamorphic stage by rapidly pinching-off from the main dorsal channel of the mid-oesophagus, an epithelial remodelling process that may be similar to other cases where epithelial tubes and vesicles arise from a pre-existing epithelial sheet. The developmental remodelling mechanism could have facilitated an abrupt evolutionary transition to the derived morphology of this important gastropod feeding innovation.

scholarly journals δ-Conotoxin SuVIA suggests an evolutionary link between ancestral predator defence and the origin of fish-hunting behaviour in carnivorous cone snails

2015 ◽  
Vol 282 (1811) ◽  
pp. 20150817 ◽  
Author(s):  
Ai-Hua Jin ◽  
Mathilde R. Israel ◽  
Marco C. Inserra ◽  
Jennifer J. Smith ◽  
Richard J. Lewis ◽  
...  
Keyword(s):  
Voltage Dependence ◽  
Venom Gland ◽  
Underlying Mechanism ◽  
Cone Snail ◽  
Evolutionary Transition ◽  
Hunting Behaviour ◽  
Defensive Role ◽  
Cone Snails ◽  
Nanomolar Range ◽  
Predator Defence

Some venomous cone snails feed on small fishes using an immobilizing combination of synergistic venom peptides that target K v and Na v channels. As part of this envenomation strategy, δ-conotoxins are potent ichtyotoxins that enhance Na v channel function. δ-Conotoxins belong to an ancient and widely distributed gene superfamily, but any evolutionary link from ancestral worm-eating cone snails to modern piscivorous species has not been elucidated. Here, we report the discovery of SuVIA, a potent vertebrate-active δ-conotoxin characterized from a vermivorous cone snail ( Conus suturatus ). SuVIA is equipotent at hNa V 1.3, hNa V 1.4 and hNa V 1.6 with EC 50 s in the low nanomolar range. SuVIA also increased peak hNa V 1.7 current by approximately 75% and shifted the voltage-dependence of activation to more hyperpolarized potentials from –15 mV to –25 mV, with little effect on the voltage-dependence of inactivation. Interestingly, the proximal venom gland expression and pain-inducing effect of SuVIA in mammals suggest that δ-conotoxins in vermivorous cone snails play a defensive role against higher order vertebrates. We propose that δ-conotoxins originally evolved in ancestral vermivorous cones to defend against larger predators including fishes have been repurposed to facilitate a shift to piscivorous behaviour, suggesting an unexpected underlying mechanism for this remarkable evolutionary transition.

scholarly journals Ero1-Mediated Reoxidation of Protein Disulfide Isomerase Accelerates the Folding of Cone Snail Toxins

2018 ◽  
Vol 19 (11) ◽  
pp. 3418 ◽  
Author(s):  
Henrik O’Brien ◽  
Shingo Kanemura ◽  
Masaki Okumura ◽  
Robert Baskin ◽  
Pradip Bandyopadhyay ◽  
...  
Keyword(s):  
Protein Disulfide Isomerase ◽  
Venom Gland ◽  
Cone Snail ◽  
Disulfide Isomerase ◽  
Folding Rates ◽  
Cone Snails ◽  
And Function ◽  
Protein Disulfide ◽  
Insight Into

Disulfide-rich peptides are highly abundant in nature and their study has provided fascinating insight into protein folding, structure and function. Venomous cone snails belong to a group of organisms that express one of the largest sets of disulfide-rich peptides (conotoxins) found in nature. The diversity of structural scaffolds found for conotoxins suggests that specialized molecular adaptations have evolved to ensure their efficient folding and secretion. We recently showed that canonical protein disulfide isomerase (PDI) and a conotoxin-specific PDI (csPDI) are ubiquitously expressed in the venom gland of cone snails and play a major role in conotoxin folding. Here, we identify cone snail endoplasmic reticulum oxidoreductin-1 (Conus Ero1) and investigate its role in the oxidative folding of conotoxins through reoxidation of cone snail PDI and csPDI. We show that Conus Ero1 preferentially reoxidizes PDI over csPDI, suggesting that the reoxidation of csPDI may rely on an Ero1-independent molecular pathway. Despite the preferential reoxidation of PDI over csPDI, the combinatorial effect of Ero1 and csPDI provides higher folding yields than Ero1 and PDI. We further demonstrate that the highest in vitro folding rates of two model conotoxins are achieved when all three enzymes are present, indicating that these enzymes may act synergistically. Our findings provide new insight into the generation of one of the most diverse classes of disulfide-rich peptides and may improve current in vitro approaches for the production of venom peptides for pharmacological studies.

scholarly journals Transcriptomic-Proteomic Correlation in the Predation-Evoked Venom of the Cone Snail, Conus imperialis

Marine Drugs ◽  
2019 ◽  
Vol 17 (3) ◽  
pp. 177 ◽  
Author(s):  
Ai-Hua Jin ◽  
Sébastien Dutertre ◽  
Mriga Dutt ◽  
Vincent Lavergne ◽  
Alun Jones ◽  
...  
Keyword(s):  
Geographical Location ◽  
Venom Gland ◽  
Feeding Habit ◽  
Poor Correlation ◽  
Stabilizing Selection ◽  
Cone Snail ◽  
Venom Composition ◽  
Cone Snails ◽  
And Gender ◽  
Labelling Method

Individual variation in animal venom has been linked to geographical location, feeding habit, season, size, and gender. Uniquely, cone snails possess the remarkable ability to change venom composition in response to predatory or defensive stimuli. To date, correlations between the venom gland transcriptome and proteome within and between individual cone snails have not been reported. In this study, we use 454 pyrosequencing and mass spectrometry to decipher the transcriptomes and proteomes of the venom gland and corresponding predation-evoked venom of two specimens of Conus imperialis. Transcriptomic analyses revealed 17 conotoxin gene superfamilies common to both animals, including 5 novel superfamilies and two novel cysteine frameworks. While highly expressed transcripts were common to both specimens, variation of moderately and weakly expressed precursor sequences was surprisingly diverse, with one specimen expressing two unique gene superfamilies and consistently producing more paralogs within each conotoxin gene superfamily. Using a quantitative labelling method, conotoxin variability was compared quantitatively, with highly expressed peptides showing a strong correlation between transcription and translation, whereas peptides expressed at lower levels showed a poor correlation. These results suggest that major transcripts are subject to stabilizing selection, while minor transcripts are subject to diversifying selection.

scholarly journals Venom Diversity and Evolution in the Most Divergent Cone Snail Genus Profundiconus

Toxins ◽  
2019 ◽  
Vol 11 (11) ◽  
pp. 623 ◽  
Author(s):  
Giulia Fassio ◽  
Maria Vittoria Modica ◽  
Lou Mary ◽  
Paul Zaharias ◽  
Alexander E. Fedosov ◽  
...  
Keyword(s):  
De Novo ◽  
Venom Gland ◽  
Phylogenetic Position ◽  
Cone Snail ◽  
Dietary Breadth ◽  
The Family ◽  
New Gene ◽  
Peptide Toxins ◽  
Transcript Diversity ◽  
Venom Evolution

Profundiconus is the most divergent cone snail genus and its unique phylogenetic position, sister to the rest of the family Conidae, makes it a key taxon for examining venom evolution and diversity. Venom gland and foot transcriptomes of Profundiconus cf. vaubani and Profundiconus neocaledonicus were de novo assembled, annotated, and analyzed for differential expression. One hundred and thirty-seven venom components were identified from P. cf. vaubani and 82 from P. neocaledonicus, with only four shared by both species. The majority of the transcript diversity was composed of putative peptides, including conotoxins, profunditoxins, turripeptides, insulin, and prohormone-4. However, there were also a significant percentage of other putative venom components such as chymotrypsin and L-rhamnose-binding lectin. The large majority of conotoxins appeared to be from new gene superfamilies, three of which are highly different from previously reported venom peptide toxins. Their low conotoxin diversity and the type of insulin found suggested that these species, for which no ecological information are available, have a worm or molluscan diet associated with a narrow dietary breadth. Our results indicate that Profundiconus venom is highly distinct from that of other cone snails, and therefore important for examining venom evolution in the Conidae family.

scholarly journals Nascent life cycles and the emergence of higher-level individuality

2017 ◽  
Vol 372 (1735) ◽  
pp. 20160420 ◽  
Author(s):  
William C. Ratcliff ◽  
Matthew Herron ◽  
Peter L. Conlin ◽  
Eric Libby
Keyword(s):  
Mathematical Modelling ◽  
Crucial Role ◽  
Early Life ◽  
Life Cycles ◽  
Levels Of Selection ◽  
Evolutionary Transition ◽  
Beneficial Mutations ◽  
Evolutionary Transitions ◽  
Key Innovation ◽  
Evolutionary Transitions In Individuality

Evolutionary transitions in individuality (ETIs) occur when formerly autonomous organisms evolve to become parts of a new, ‘higher-level’ organism. One of the first major hurdles that must be overcome during an ETI is the emergence of Darwinian evolvability in the higher-level entity (e.g. a multicellular group), and the loss of Darwinian autonomy in the lower-level units (e.g. individual cells). Here, we examine how simple higher-level life cycles are a key innovation during an ETI, allowing this transfer of fitness to occur ‘for free’. Specifically, we show how novel life cycles can arise and lead to the origin of higher-level individuals by (i) mitigating conflicts between levels of selection, (ii) engendering the expression of heritable higher-level traits and (iii) allowing selection to efficiently act on these emergent higher-level traits. Further, we compute how canonical early life cycles vary in their ability to fix beneficial mutations via mathematical modelling. Life cycles that lack a persistent lower-level stage and develop clonally are far more likely to fix ‘ratcheting’ mutations that limit evolutionary reversion to the pre-ETI state. By stabilizing the fragile first steps of an evolutionary transition in individuality, nascent higher-level life cycles may play a crucial role in the origin of complex life. This article is part of the themed issue ‘Process and pattern in innovations from cells to societies’.

scholarly journals Rapid sensitive analysis of cysteine rich peptide venom components

2009 ◽  
Vol 106 (17) ◽  
pp. 6910-6915 ◽  
Author(s):  
Beatrix M. Ueberheide ◽  
David Fenyö ◽  
Paul F. Alewood ◽  
Brian T. Chait
Keyword(s):  
Charge State ◽  
Disulfide Bonds ◽  
Electron Transfer Dissociation ◽  
Venom Gland ◽  
Bioactive Molecules ◽  
Sequence Information ◽  
Cone Snail ◽  
Sequence Coverage ◽  
Crude Venom ◽  
Peptide Toxins

Disulfide-rich peptide venoms from animals such as snakes, spiders, scorpions, and certain marine snails represent one of nature's great diversity libraries of bioactive molecules. The various species of marine cone shells have alone been estimated to produce >50,000 distinct peptide venoms. These peptides have stimulated considerable interest because of their ability to potently alter the function of specific ion channels. To date, only a small fraction of this immense resource has been characterized because of the difficulty in elucidating their primary structures, which range in size between 10 and 80 aa, include up to 5 disulfide bonds, and can contain extensive posttranslational modifications. The extraordinary complexity of crude venoms and the lack of DNA databases for many of the organisms of interest present major analytical challenges. Here, we describe a strategy that uses mass spectrometry for the elucidation of the mature peptide toxin components of crude venom samples. Key to this strategy is our use of electron transfer dissociation (ETD), a mass spectrometric fragmentation technique that can produce sequence information across the entire peptide backbone. However, because ETD only yields comprehensive sequence coverage when the charge state of the precursor peptide ion is sufficiently high and the m/z ratio is low, we combined ETD with a targeted chemical derivatization strategy to increase the charge state of cysteine-containing peptide toxins. Using this strategy, we obtained full sequences for 31 peptide toxins, using just 7% of the crude venom from the venom gland of a single cone snail (Conus textile).

scholarly journals Combined Proteotranscriptomic-Based Strategy to Discover Novel Antimicrobial Peptides from Cone Snails

Biomedicines ◽  
2021 ◽  
Vol 9 (4) ◽  
pp. 344
Author(s):  
Anicet Ebou ◽  
Dominique Koua ◽  
Audrey Addablah ◽  
Solange Kakou-Ngazoa ◽  
Sébastien Dutertre
Keyword(s):  
Antimicrobial Peptides ◽  
Marine Invertebrates ◽  
Current Knowledge ◽  
Venom Gland ◽  
Biologically Active ◽  
Cone Snail ◽  
Active Peptides ◽  
Speed Up ◽  
Cone Snails ◽  
Conventional Antibiotics

Despite their impressive diversity and already broad therapeutic applications, cone snail venoms have received less attention as a natural source in the investigation of antimicrobial peptides than other venomous animals such as scorpions, spiders, or snakes. Cone snails are among the largest genera (Conus sp.) of marine invertebrates, with more than seven hundred species described to date. These predatory mollusks use their sophisticated venom apparatus to capture prey or defend themselves. In-depth studies of these venoms have unraveled many biologically active peptides with pharmacological properties of interest in the field of pain management, the treatment of epilepsy, neurodegenerative diseases, and cardiac ischemia. Considering sequencing efficiency and affordability, cone snail venom gland transcriptome analyses could allow the discovery of new, promising antimicrobial peptides. We first present here the need for novel compounds like antimicrobial peptides as a viable alternative to conventional antibiotics. Secondly, we review the current knowledge on cone snails as a source of antimicrobial peptides. Then, we present the current state of the art in analytical methods applied to crude or milked venom followed by how antibacterial activity assay can be implemented for fostering cone snail antimicrobial peptides studies. We also propose a new innovative profile Hidden Markov model-based approach to annotate full venom gland transcriptomes and speed up the discovery of potentially active peptides from cone snails.

scholarly journals Going underwater: multiple origins and functional morphology of piercing-sucking feeding and tracheal system adaptations in water scavenger beetle larvae (Coleoptera: Hydrophiloidea)

2020 ◽  
Author(s):  
Georgina Rodriguez ◽  
Martin Fikáček ◽  
Yȗsuke N Minoshima ◽  
Miguel Archangelsky ◽  
Patricia L M Torres
Keyword(s):  
Functional Morphology ◽  
Feeding Behaviour ◽  
Sem Analysis ◽  
Feeding Strategies ◽  
Aquatic Habitats ◽  
Tracheal System ◽  
Multiple Origins ◽  
Key Innovation ◽  
Evolutionary Aspects ◽  
Character Mapping

Abstract Larvae of water scavenger beetles (Coleoptera: Hydrophiloidea) are adapted to a wide variety of aquatic habitats, but little is known about functional and evolutionary aspects of these adaptations. We review the functional morphology and evolution of feeding strategies of larvae of the families Hydrophilidae and Epimetopidae based on a detailed scanning electron microscope (SEM) analysis, analysis of video records of feeding behaviour and observations of living larvae. There are two main types of feeding mechanisms: chewing and piercing-sucking. The character mapping using the latest phylogenetic hypothesis for Hydrophiloidea infers the chewing system as the ancestral condition. The piercing-sucking mechanism evolved at least four times independently: once in Epimetopidae (Epimetopus) and three times in Hydrophilidae (Berosini: Berosus + Hemiosus; Laccobiini: Laccobius group; Hydrobiusini: Hybogralius). The piercing-sucking apparatus allows underwater extra-oral digestion and decreases the dependence of larvae on an aerial environment. A detailed study of the tracheal morphology of the piercing-sucking lineages reveals four independent origins of the apneustic respiratory system, all of them nested within lineages with piercing-sucking mouthparts. We conclude that piercing-sucking mouthparts represent a key innovation, which allows for the subsequent adaptation of the tracheal system, influences the diversification dynamics of the lineages and allows the shift to new adaptive zones.

Uncovering Intense Protein Diversification in a Cone Snail Venom Gland Using an Integrative Venomics Approach

2015 ◽  
Vol 14 (2) ◽  
pp. 628-638 ◽  
Author(s):  
Daniel Biass ◽  
Aude Violette ◽  
Nicolas Hulo ◽  
Frédérique Lisacek ◽  
Philippe Favreau ◽  
...  
Keyword(s):  
Venom Gland ◽  
Cone Snail

scholarly journals Synthesis, Pharmacological and Structural Characterization of Novel Conopressins from Conus miliaris

Marine Drugs ◽  
2020 ◽  
Vol 18 (3) ◽  
pp. 150 ◽  
Author(s):  
Julien Giribaldi ◽  
Lotten Ragnarsson ◽  
Tom Pujante ◽  
Christine Enjalbal ◽  
David Wilson ◽  
...  
Keyword(s):  
Partial Agonist ◽  
Venom Gland ◽  
Membrane Receptors ◽  
Cone Snail ◽  
Critical Position ◽  
Pharmacological Characterization ◽  
Novel Structure ◽  
Drug Lead ◽  
A Charge

Cone snails produce a fast-acting and often paralyzing venom, largely dominated by disulfide-rich conotoxins targeting ion channels. Although disulfide-poor conopeptides are usually minor components of cone snail venoms, their ability to target key membrane receptors such as GPCRs make them highly valuable as drug lead compounds. From the venom gland transcriptome of Conus miliaris, we report here on the discovery and characterization of two conopressins, which are nonapeptide ligands of the vasopressin/oxytocin receptor family. These novel sequence variants show unusual features, including a charge inversion at the critical position 8, with an aspartate instead of a highly conserved lysine or arginine residue. Both the amidated and acid C-terminal analogues were synthesized, followed by pharmacological characterization on human and zebrafish receptors and structural investigation by NMR. Whereas conopressin-M1 showed weak and only partial agonist activity at hV1bR (amidated form only) and ZFV1a1R (both amidated and acid form), both conopressin-M2 analogues acted as full agonists at the ZFV2 receptor with low micromolar affinity. Together with the NMR structures of amidated conopressins-M1, -M2 and -G, this study provides novel structure-activity relationship information that may help in the design of more selective ligands.

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