Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus
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Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus. / Aman, Joseph W; Imperial, Julita S; Ueberheide, Beatrix; Zhang, Min-Min; Aguilar, Manuel; Taylor, Dylan; Watkins, Maren; Yoshikami, Doju; Showers-Corneli, Patrice; Safavi-Hemami, Helena; Biggs, Jason; Teichert, Russell W; Olivera, Baldomero M.
I: Proceedings of the National Academy of Sciences of the United States of America, Bind 112, Nr. 16, 2015, s. 5087-5092.Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › fagfællebedømt
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TY - JOUR
T1 - Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus
AU - Aman, Joseph W
AU - Imperial, Julita S
AU - Ueberheide, Beatrix
AU - Zhang, Min-Min
AU - Aguilar, Manuel
AU - Taylor, Dylan
AU - Watkins, Maren
AU - Yoshikami, Doju
AU - Showers-Corneli, Patrice
AU - Safavi-Hemami, Helena
AU - Biggs, Jason
AU - Teichert, Russell W
AU - Olivera, Baldomero M
PY - 2015
Y1 - 2015
N2 - Prey shifts in carnivorous predators are events that can initiate the accelerated generation of new biodiversity. However, it is seldom possible to reconstruct how the change in prey preference occurred. Here we describe an evolutionary "smoking gun" that illuminates the transition from worm hunting to fish hunting among marine cone snails, resulting in the adaptive radiation of fish-hunting lineages comprising ∼100 piscivorous Conus species. This smoking gun is δ-conotoxin TsVIA, a peptide from the venom of Conus tessulatus that delays inactivation of vertebrate voltage-gated sodium channels. C. tessulatus is a species in a worm-hunting clade, which is phylogenetically closely related to the fish-hunting cone snail specialists. The discovery of a δ-conotoxin that potently acts on vertebrate sodium channels in the venom of a worm-hunting cone snail suggests that a closely related ancestral toxin enabled the transition from worm hunting to fish hunting, as δ-conotoxins are highly conserved among fish hunters and critical to their mechanism of prey capture; this peptide, δ-conotoxin TsVIA, has striking sequence similarity to these δ-conotoxins from piscivorous cone snail venoms. Calcium-imaging studies on dissociated dorsal root ganglion (DRG) neurons revealed the peptide's putative molecular target (voltage-gated sodium channels) and mechanism of action (inhibition of channel inactivation). The results were confirmed by electrophysiology. This work demonstrates how elucidating the specific interactions between toxins and receptors from phylogenetically well-defined lineages can uncover molecular mechanisms that underlie significant evolutionary transitions.
AB - Prey shifts in carnivorous predators are events that can initiate the accelerated generation of new biodiversity. However, it is seldom possible to reconstruct how the change in prey preference occurred. Here we describe an evolutionary "smoking gun" that illuminates the transition from worm hunting to fish hunting among marine cone snails, resulting in the adaptive radiation of fish-hunting lineages comprising ∼100 piscivorous Conus species. This smoking gun is δ-conotoxin TsVIA, a peptide from the venom of Conus tessulatus that delays inactivation of vertebrate voltage-gated sodium channels. C. tessulatus is a species in a worm-hunting clade, which is phylogenetically closely related to the fish-hunting cone snail specialists. The discovery of a δ-conotoxin that potently acts on vertebrate sodium channels in the venom of a worm-hunting cone snail suggests that a closely related ancestral toxin enabled the transition from worm hunting to fish hunting, as δ-conotoxins are highly conserved among fish hunters and critical to their mechanism of prey capture; this peptide, δ-conotoxin TsVIA, has striking sequence similarity to these δ-conotoxins from piscivorous cone snail venoms. Calcium-imaging studies on dissociated dorsal root ganglion (DRG) neurons revealed the peptide's putative molecular target (voltage-gated sodium channels) and mechanism of action (inhibition of channel inactivation). The results were confirmed by electrophysiology. This work demonstrates how elucidating the specific interactions between toxins and receptors from phylogenetically well-defined lineages can uncover molecular mechanisms that underlie significant evolutionary transitions.
KW - Amino Acid Sequence
KW - Animals
KW - Biological Assay
KW - Conotoxins/chemistry
KW - Conus Snail/anatomy & histology
KW - Fishes/physiology
KW - Molecular Sequence Data
KW - Peptides/metabolism
KW - Phylogeny
KW - Predatory Behavior/physiology
U2 - 10.1073/pnas.1424435112
DO - 10.1073/pnas.1424435112
M3 - Journal article
C2 - 25848010
VL - 112
SP - 5087
EP - 5092
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 16
ER -
ID: 232824243