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Fine structure of the silk spinning system in the caddisworm, Hydatophylax nigrovittatus (Trichoptera: Limnephilidae)

  • Hyo-Jeong Kim (Department of Biological Sciences, Dankook University) ;
  • Yan Sun (Department of Biological Sciences, Dankook University) ;
  • Myung-Jin Moon (Department of Biological Sciences, Dankook University)
  • Received : 2020.06.26
  • Accepted : 2020.07.28
  • Published : 2020.12.31

Abstract

Silk is produced by a variety of insects, but only silk made by terrestrial arthropods has been examined in detail. To fill the gap, this study was designed to understand the silk spinning system of aquatic insect. The larvae of caddis flies, Hydatophylax nigrovittatus produce silk through a pair of labial silk glands and use raw silk to protect themselves in the aquatic environment. The result of this study clearly shows that although silk fibers are made under aquatic conditions, the cellular silk production system is quite similar to that of terrestrial arthropods. Typically, silk production in caddisworm has been achieved by two independent processes in the silk glands. This includes the synthesis of silk fibroin in the posterior region, the production of adhesive glycoproteins in the anterior region, which are ultimately accumulated into functional silk dope and converted to a silk ribbon coated with gluey substances. At the cellular level, each substance of fibroin and glycoprotein is specifically synthesized at different locations, and then transported from the rough ER to the Golgi apparatus as transport vesicles, respectively. Thereafter, the secretory vesicles gradually increase in size by vesicular fusion, forming larger secretory granules containing specific proteins. It was found that these granules eventually migrate to the apical membrane and are exocytosed into the lumen by a mechanism of merocrine secretion.

Keywords

Acknowledgement

This research was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2019R1I1A3A01062105).

References

  1. H. Akai, in The Ultrastructure and Functions of the Silk Gland Cells of Bombyx mori, ed. by R. C. King, H. Akai. Insect ultrastructure (Springer, Boston, 1984), pp. 323-364
  2. H. Akai, M. Kobayash, Incorporation of labeled thymidine into the silk gland of the silkworm. Nature 206, 847-848 (1965)
  3. N.N. Ashton, R.J. Stewart, Aquatic caddisworm silk is solidified by environmental metal ions during the natural fiber-spinning process. FASEB J. 33, 572-583 (2019)
  4. N.N. Ashton, D. Taggart, R.J. Stewart, Silk tape nanostructure and silk gland anatomy of trichoptera. Biopolymers 97, 432-445 (2012)
  5. N.N. Ashton, C. Wang, R.J. Stewart, in The Adhesive Tape-like Silk of Aquatic Caddisworms. Biological adhesives (Springer, Berlin, 2016), pp. 107-128
  6. S. Busse, T.H. Buscher, K.E. Taylor, L. Heepe, J.S. Edgerly, S.N. Gorb, Pressureinduced silk spinning mechanism in webspinners (Insecta: Embioptera). Soft Matter 47, 9742-9750 (2019)
  7. C.L. Craig, Evolution of arthropod silks. Annu. Rev. Entomol. 42, 231-267 (1997)
  8. S.C. Crew, B. Opell, The features of capture threads and orb-webs produced by unfed Cuyclosa turbinata (Araneae: Araneidae). J. Arachnol. 34, 427-434 (2006)
  9. M.S. Engster, Studies on silk secretion in the Trichoptera (F. Limnephidae). I. Histology, histochemistry, and ultrastructure of the silk glands. Cell Tissue Res. 169, 77-92 (1976)
  10. H. Kim, J.K. Seo, K.J. Kim, K.H. Chung, M.J. Moon, Fine structural reconstruction on the testicular cyst of the furrow orb weaver Larinioides cornutus by 3D volume rendering. Anim. Cells Sys. 20, 267-275 (2016)
  11. J. Kovoor, in Comparative Structure and Histochemistry of Silk-Producing Organs in Arachnids, ed. by W. Nentwig. Ecophysiology of spiders (Springer-Verlag, Berlin, 1987), pp. 159-186
  12. K. Kronenberger, C. Dicko, F. Vollrath, A novel marine silk. Naturwissenschaften 99, 3-12 (2012)
  13. M.J. Moon, Fine structure of the aggregate silk nodules in the orb-web spider Nephila clavata. Anim. Cells Sys. 22, 421-428 (2018)
  14. M.J. Moon, J.G. Park, Spinning apparatus for the dragline silk in the funnel-web spider Agelena limbata (Araneae: Agelenidae). Anim. Cells Sys. 12, 109-116 (2008)
  15. M.J. Moon, E.K. Tillinghast, Fine structure of the glandular epithelium during secretory silk production in the black widow spider, Latrodectus mactans. Kor. J. Biol. Sci. 6, 327-333 (2002)
  16. M.J. Moon, E.K. Tillinghast, Silk production after mechanical pulling stimulation in the ampullate silk glands of the barn spider, Araneus cavaticus. Entomol. Res. 34, 123-130 (2004)
  17. M.J. Moon, S.C. Yang, Microstructure of pretarsal pulvilli in the shield bug Acanthosoma spinicolle (Heteroptera: Acanthosomatidae). Entomol. Res. 44, 199-206 (2014)
  18. J.P. O'Brien, S.R. Fahnestock, Y. Termonia, K.H. Gardner, Nylons from nature: Synthetic analogs to spider silk. Adv. Mater. 10, 1185-1195 (1998)
  19. K. Ohkawa, T. Nomura, R. Arai, K. Abe, M. Tsukada, K. Hirabayashi, in Characterization of Underwater Silk Proteins from Caddisfly Larva, Stenopsyche marmorata, ed. by T. Asakura, T. Miller. Biotechnology of silk - biologically-inspired systems, vol 5 (Springer, Dordrecht, 2014)
  20. J.G. Park, M.J. Moon, Fine structural analysis on triad spinning spigots of an orbweb spider's capture threads. Entomol. Res. 44, 121-129 (2014)
  21. K.M. Rudall, W. Kenchington, Arthropod silks: The problem of fibrous proteins in animal tissues. Annu. Rev. Entomol. 16, 73-96 (1971)
  22. S. Sasaki, E. Nakajima, Y. Fujii-Kuriyama, Y. Tashiro, Intracellular transport and secretion of fibroin in the posterior silk gland of the silkworm Bombyx mori. J. Cell Sci. 50, 19-44 (1981)
  23. F. Sehnal, H. Akai, Insect silk glands: Their types, development and function, and effects of environmental factors and morphogenetic hormones on them. J. Insect Morphol. Embryol. 19, 79-132 (1990)
  24. F. Sehnal, T. Sutherland, Silks produced by insect labial glands. Prion 2, 145-153 (2008)
  25. R.J. Stewart, C.S. Wang, Adaptation of caddisfly larval silks to aquatic habitats by phosphorylation of H-fibroin serines. Biomacromolecules 11, 969-974 (2010)
  26. T.D. Sutherland, J.H. Young, S. Weisman, C.Y. Hayashi, D.J. Merritt, Insect silk: One name, many materials. Annu. Rev. Entomol. 55, 171-188 (2010)
  27. E.K. Tillinghast, M. Townley, The independent regulation of protein synthesis in the major ampullate glands of Araneus cavaticus Keyserling. J. Insect Physiol. 32, 117-123 (1986)
  28. A.R. Tindall, The larval case of Triaenodes bicolor Curtis (Trichoptera: Leptoceridae). Proc. Roy. Ent. Soc. Lond. A 35, 93-96 (1960)
  29. M. Tszydel, A. Zablotni, D. Wojciechowska, M. Michalak, I. Krucinska, K. Szustakiewicz, M. Maj, A. Jaruszewska, J. Strzelecki, Research on possible medical use of silk produced by caddisfly larvae of Hydropsyche angustipennis (Trichoptera, Insecta). J. Mech. Behav. Biomed. Mater. 45, 142-153 (2015)
  30. F. Vollrath, D.P. Knight, Liquid crystalline spinning of spider silk. Nature 410, 541-548 (2001)
  31. F. Vollrath, E.K. Tillinghast, Glycoprotein glue beneath a spider web's aqueous coat. Naturwissenschaften 78, 557-559 (1991)
  32. A.A. Walker, S. Weisman, J.S. Church, D.J. Merritt, S.T. Mudie, T.D. Sutherland, Silk from crickets: A new twist on spinning. PLoS One 7, e30408 (2012)
  33. A. Weiskopf, K. Senecal, P. Vouros, D. Kaplan, C.M. Mello, The carbohydrate composition of spider silk: Nephila edulis dragline. Glycobiology 6, 1703-1708 (1996)
  34. G.B. Wiggins, Caddisflies: The Underwater Architects (University of Toronto Press, Toronto, 2004)
  35. J.H. Yang, D.J. Merritt, The ultrastructure of the silk-producing basitarsus in the Hilarini (Diptera: Empidinae). Arthropod Struct. Dev. 32, 157-165 (2003)
  36. N. Yonemura, K. Mita, T. Tamura, F. Sehnal, Conservation of silk genes in Trichoptera and Lepidoptera. J. Mol. Evol. 68, 641-653 (2009)