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.
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.
Bandel, K., 1984. The Radulae of Caribbean and Other Mesogastropoda and Neogastropoda. EJ Brill, Leiden, 1–199.
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.
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.
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.
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.
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.
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.
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).
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.
Endean, R., 1972. Aspects of molluscan pharmacology. Chemical Zoology, 7: 421–466.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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).
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.
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.
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.
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.
Percharde, P. L., 1972. Observations on the gastropod, Charonia variegata, in Trinidad and Tobago. Nautilus, 85: 84–92.
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.
Poulsen, A. L., 1995. Coral reef gastropods — A sustainable resource?. Pacific Conservation Biology, 2: 142–145.
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.
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.
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.
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.
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.
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
Corresponding author
Rights and permissions
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-023-5147-y