Skip to main content

Advertisement

Log in

Identification and Expression of the Conotoxin Homologous Genes in the Giant Triton Snail (Charonia tritonis)

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

Conotoxin (CTX) is a small peptide toxin, and plays crucial role in anesthetizes prey, preys and defends competitors. Charonia tritonis is the natural predator of the crown of thorns starfish (CoTS) and the protector of coral reefs. It plays an important role in the coral reef ecosystem. However, the types of toxins produced by tritons and the molecular mechanisms of toxin secretion of C. tritonis are unknown. In the present study, the four conotoxin homologous genes (CTXs) from C. tritonis were identified. Species and conotoxin superfamily phylogenetic tree indicated that CTX-1 (CL2216.Contig2) and CTX-4 (Unigene 58438_All) belong to the C superfamily, CTX-2 (Unigene 66414_All) belong to the V superfamily, and CTX-3 (Unigene 21408_All) belong to the B1 superfamily. CTXs were highly expressed in salivary gland, liver and digestive gland. The predation control experiment revealed that the expressions of CTXs were significantly different in salivary gland, liver and digestive gland. The results indicated that CTXs may participate in the process of C. tritonis predating CoTs, and provided a scientific basis for further studying the toxins secretion mechanism of C. tritonis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abalde, S., Tenorio, M. J., Afonso, C. M. L., and Zardoya, R., 2018. Conotoxin diversity in Chelyconus ermineus (Born, 1778) and the convergent origin of piscivory in the Atlantic and Indo-Pacific cones. Genome Biology and Evolution, 10(10): 2643–2662, DOI: https://doi.org/10.1093/gbe/evy150.

    Article  Google Scholar 

  • Bandel, K., 1984. The Radulae of Caribbean and Other Mesogastropoda and Neogastropoda. EJ Brill, Leiden, 1–199.

    Google Scholar 

  • Biggs, J. S., Watkins, M., Puillandre, N., Ownby, J. P., Lopez-Vera, E., Christensen, S., et al., 2010. Evolution of Conus peptide toxins: Analysis of Conus californicus Reeve, 1844. Molecular Phylogenetics and Evolution, 56(1): 1–12, DOI: https://doi.org/10.1016/j.ympev.2010.03.029.

    Article  Google Scholar 

  • Bose, U., Suwansa-Ard, S., Maikaeo, L., Motti, C. A., Hall, M. R., and Cummins, S. F., 2017a. Neuropeptides encoded within a neural transcriptome of the giant triton snail Charonia tritonis, a Crown-of-Thorns Starfish predator. Peptides, 98: 3–14, DOI: https://doi.org/10.1016/j.peptides.2017.01.004.

    Article  Google Scholar 

  • Bose, U., Wang, T., Zhao, M., Motti, C. A., Hall, M. R., and Cummins, S. F., 2017b. Multiomics analysis of the giant triton snail salivary gland, a crown-of-thorns starfish predator. Scientific Reports, 7: 6000, DOI: https://doi.org/10.1038/s41598-017-05974-x.

    Article  Google Scholar 

  • Brown, E., Masinde, E. L. K., and Woodcock, B. G., 2016. Effects of conopeptide-containing venom from seven species of Conidae gastropoda on the chick biventer-cervicis nerve-muscle assessed using the ConoServer database. International Journal of Clinical Pharmacology and Therapeutics, 54(7): 544–554, DOI: https://doi.org/10.5414/cp202667.

    Article  Google Scholar 

  • Chesher, R. H., 1969. Destruction of Pacific corals by sea star Acanthaster planci. Science, 165(3890): 280–283, DOI: https://doi.org/10.1126/science.165.3890.280.

    Article  Google Scholar 

  • Cowan, Z. L., Pratchett, M., Messmer, V., and Ling, S., 2017. Known predators of crown-of-thorns starfish (Acanthaster spp.) and their role in mitigating, if not preventing, population outbreaks. Diversity Basel, 9(1): 7, DOI: https://doi.org/10.3390/d9010007.

    Article  Google Scholar 

  • Cui, L. B., Lu, Y. H., Liu, C. L., and Tang, H., 2000. Light and electron microscopic studies on the salivary glands of Haliotis discus hannai Ino. Acta Oceanologica Sinica, 22(1): 141–144 (in Chinese with English abstract).

    Google Scholar 

  • Dutertre, S., Jin, A. H., Kaas, Q., Jones, A., Alewood, P. F., and Lewis, R. J., 2013. Deep venomics reveals the mechanism for expanded peptide diversity in cone snail venom. Molecular & Cellular Proteomics, 12(2): 312–329, DOI: https://doi.org/10.1074/mcp.M112.021469.

    Article  Google Scholar 

  • Endean, R., 1972. Aspects of molluscan pharmacology. Chemical Zoology, 7: 421–466.

    Google Scholar 

  • Garcia Ortega, L., Alegre Cebollada, J., Garcia Linares, S., Bruix, M., Martinez del Pozo, A., and Gavilanes, J. G., 2011. The behavior of sea anemone actinoporins at the water-membrane interface. Biochimica et Biophysica Acta Biomembranes, 1808(9): 2275–2288, DOI: https://doi.org/10.1016/j.bbamem.2011.05.012.

    Article  Google Scholar 

  • Hall, A. E., and Kingsford, M. J., 2016. Variation in the population demographics of Scolopsis bilineatus in response to predators. Coral Reefs, 35(4): 1173–1185, DOI: https://doi.org/10.1007/s00338-016-1486-0.

    Article  Google Scholar 

  • Hall, M. R., Kocot, K. M., Baughman, K. W., Fernandez-Valverde, S. L., Gauthier, M. E. A., Hatleberg, W. L., et al., 2017. The crown-of-thorns starfish genome as a guide for biocontrol of this coral reef pest. Nature, 544(7649): 231–234, DOI: https://doi.org/10.1038/nature22033.

    Article  Google Scholar 

  • Kaas, Q., Westermann, J. C., and Craik, D. J., 2010. Conopeptide characterization and classifications: An analysis using ConoServer. Toxicon, 55(8): 1491–1509, DOI: https://doi.org/10.1016/j.toxicon.2010.03.002.

    Article  Google Scholar 

  • Kaas, Q., Westermann, J. C., Halai, R., Wang, C. K. L., and Craik, D. J., 2008. ConoServer, a database for conopeptide sequences and structures. Bioinformatics, 24(3): 445–446, DOI: https://doi.org/10.1093/bioinformatics/btm596.

    Article  Google Scholar 

  • Kaas, Q., Yu, R., Jin, A. H., Dutertre, S., and Craik, D. J., 2012. ConoServer: Updated content, knowledge, and discovery tools in the conopeptide database. Nucleic Acids Research, 40(D1): D325–D330, DOI: https://doi.org/10.1093/nar/gkr886.

    Article  Google Scholar 

  • Kang, K. H., and Kim, J. M., 2004. The predation of trumpet shell, Charonia sp., on eight different marine invertebrate species. Aquaculture Research, 35(13): 1202–1206, DOI: https://doi.org/10.1111/j.1365-2109.2004.01124.x.

    Article  Google Scholar 

  • Li, Q., Barghi, N., Lu, A., Fedosov, A. E., Bandyopadhyay, P. K., Lluisma, A. O., et al., 2017. Divergence of the venom exogene repertoire in two sister species of turriconus. Genome Biology and Evolution, 9(9): 2211–2225, DOI: https://doi.org/10.1093/gbe/evx157.

    Article  Google Scholar 

  • Luo, S. L., Christensen, S., Zhangsun, D. T., Wu, Y., Hu, Y., Zhu, X. P., et al., 2013. A novel inhibitor of α9α10 nicotinic acetylcholine receptors from Conus vexillum delineates a new conotoxin superfamily. PLoS One, 8(1): e54648, DOI: https://doi.org/10.1371/journal.pone.0054648.

    Article  Google Scholar 

  • Luo, S. L., Wu, Y., Zhu, X. P., and Feng, J. C., 2007. Cloning of novel O-superfamily conotoxin of Conus capitaneus collected from Hainan. Chinese Journal of Marine Drugs, 26(1): 1–7 (in Chinese with English abstract).

    Google Scholar 

  • Lynch, S. S., Cheng, C. M., and Yee, J. L., 2006. Intrathecal ziconotide for refractory chronic pain. Annals of Pharmacotherapy, 40(7–8): 1293–1300, DOI: https://doi.org/10.1345/aph.1G584.

    Article  Google Scholar 

  • McGivern, J. G., 2007. Ziconotide: A review of its pharmacology and use in the treatment of pain. Neuropsychiatric Disease and Treatment, 3(1): 69–85, DOI: https://doi.org/10.2147/nedt.2007.3.1.69.

    Article  Google Scholar 

  • Miljanich, G. P., 2004. Ziconotide: Neuronal calcium channel blocker for treating severe chronic pain. Current Medicinal Chemistry, 11(23): 3029–3040, DOI: https://doi.org/10.2174/0929867043363884.

    Article  Google Scholar 

  • Peng, C., Yao, G., Gao, B. M., Fan, C. X., Bian, C., Wang, J. T., et al., 2016. High-throughput identification of novel conotoxins from the Chinese tubular cone snail (Conus betulinus) by multi-transcriptome sequencing. Gigascience, 5: 17, DOI: https://doi.org/10.1186/s13742-016-0122-9.

    Article  Google Scholar 

  • Percharde, P. L., 1972. Observations on the gastropod, Charonia variegata, in Trinidad and Tobago. Nautilus, 85: 84–92.

    Google Scholar 

  • Phuong, M. A., Mahardika, G. N., and Alfaro, M. E., 2016. Dietary breadth is positively correlated with venom complexity in cone snails. BMC Genomics, 17: 401, DOI: https://doi.org/10.1186/s12864-016-2755-6.

    Article  Google Scholar 

  • Poulsen, A. L., 1995. Coral reef gastropods — A sustainable resource?. Pacific Conservation Biology, 2: 142–145.

    Article  Google Scholar 

  • Robinson, S. D., Li, Q., Lu, A., Bandyopadhyay, P. K., Yandell, M., Olivera, B. M., et al., 2017. The venom repertoire of Conus gloriamaris (Chemnitz, 1777), the glory of the sea. Marine Drugs, 15(5): 145, DOI: https://doi.org/10.3390/md15050145.

    Article  Google Scholar 

  • Safavi-Hemami, H., Siero, W. A., Gorasia, D. G., Young, N. D., Macmillan, D., Williamson, N. A., et al., 2011. Specialisation of the venom gland proteome in predatory cone snails reveals functional diversification of the conotoxin biosynthetic pathway. Journal of Proteome Research, 10(9): 3904–3919, DOI: https://doi.org/10.1021/pr1012976.

    Article  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S., 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology & Evolution, 30(12): 2725–2729.

    Article  Google Scholar 

  • Zhang, G. G., Xu, M., Zhang, C. L., Jia, H. X., Zhang, H., He, M. X., et al., 2021. Comparative transcriptomic and expression profiles between the foot muscle and mantletissues in the giant triton snail Charonia tritonis. Frontiers in Physiology, 12: 632 518, DOI: https://doi.org/10.3389/fphys.2021.632518.

    Google Scholar 

  • Zhang, L. P., Xia, J., Peng, P. F., Li, P., Luo, P., and Hu, C. Q., 2013. Characterization of embryogenesis and early larval development in the Pacific triton, Charonia tritonis (Gastropoda: Caenogastropoda). Invertebrate Reproduction & Development, 57(3): 237–246, DOI: https://doi.org/10.1080/07924259.2012.753472.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 42176129), the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA13020206), the Key Special Project for Introduced Talents Team of Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (No. GML2019ZD0402), and the Planning Project of Guangdong Province, China, Guangdong Provincial Key Laboratory of Applied Marine Biology (No. 2020B1212060058).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenguang Liu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, H., Zhang, G., Zhang, C. et al. Identification and Expression of the Conotoxin Homologous Genes in the Giant Triton Snail (Charonia tritonis). J. Ocean Univ. China 22, 213–220 (2023). https://doi.org/10.1007/s11802-023-5147-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-023-5147-y

Key words

Navigation