The Biological Activity of Extracts of Marine Invertebrates from Troitsa Bay (Sea of Japan)


The biological activity of extracts from nine species of marine invertebrates (the phyla Cnidaria, Annelida, Sipunculida, and Nemertea) that inhabit Troitsa Bay (Peter the Great Bay, Sea of Japan) was determined using in vitro and in vivo models. It was found that extracts of marine worms, that is, the polychaete Eularia viridis and sipunculida Phascolostoma agassizii, have an antibacterial effect and reduce the adhesion of macrophages, whereas extracts of the jellyfish Gonionemus vertens exhibit neurotoxic effects and are also able to increase or decrease the adhesion of macrophages, depending on the method of extraction. These marine animals can be a source of antimicrobial, antioxidant, antitumor, and immunostimulating compounds.

This is a preview of subscription content, access via your institution.


  1. 1

    Alonso-del-Rivero, M., Trejo, S., Rodríguez de la Vega, M., et al., A novel metallocarboxypeptidase-like enzyme from the marine annelid Sabellastarte magnifica—a step into the invertebrate world of proteases, FEBS J., 2009, vol. 276, pp. 4875−4890.

    Article  CAS  PubMed  Google Scholar 

  2. 2

    Alonso-del-Rivero, M., Trejo, S., and Reytor, M.L., Tri-domain bifunctional inhibitor of metallocarboxypeptidases A and serine proteinases isolated from marine annelid Sabellastarte magnifica, J. Biol. Chem., 2012, vol. 287, no. 19, pp. 15427−15438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Andersson, H., Jacobsson, E., Strand, M., et al., α‑Nemertides, a novel family of marine peptide neurotoxins from ribbon worms, 19th World Congress of the IST, Haikou, People’s Republic of China, Oct. 24−31, 2017, p. 138.

  4. 4

    Bacq, Z., Poisons of nemerteans, Bull. Acad. R. Belg. Cl. Sci., 1936, vol. 22, pp. 1072−1079.

    Google Scholar 

  5. 5

    Badré, S., Bioactive toxins from stinging jellyfish, Toxicon, 2014, vol. 1, pp. 11−12.

    Google Scholar 

  6. 6

    Baurain, D., Brinkmann, H., and Philippe, H., Lack of resolution in the animal phylogeny: closely spaced cladogeneses or undetected systematic errors?, Mol. Biol. Evol., 2007, vol. 24, no. 1, pp. 6−9.

    Article  CAS  PubMed  Google Scholar 

  7. 7

    Boore, J., Lavrov, D., and Brown, W., Gene translocation links insects and crustaceans, Nature, 1998, vol. 392, pp. 667−668.

    Article  CAS  PubMed  Google Scholar 

  8. 8

    Carmichael, J., Degraff, W.G., Gazdar, A.F., et al., Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing, Cancer Res., 1987, vol. 47, pp. 936−942.

    CAS  PubMed  Google Scholar 

  9. 9

    Carroll, S., McEvoy, E., Gibson, R., et al., The production of tetrodotoxin-like substances by nemertean worms in conjunction with bacteria, J. Exp. Mar. Biol. Ecol., 2002, vol. 288, pp. 51−63.

    Article  CAS  Google Scholar 

  10. 10

    Cooper, E., Comparative Immunology, Englewood Cliffs, N.J.: Prentice Hall, 1976, pp. 88, 103, 202, and 274.

    Google Scholar 

  11. 11

    Florkin, M., Chemical Zoology, vol. 4: Annelida, Echiuria, and Sipuncula, New York: Academic, 1969, pp. 420−437.

    Google Scholar 

  12. 12

    Glinsky, G., Anti-adhesion cancer therapy, Cancer Metastasis Rev., 1998, vol. 17, pp. 177−185.

    Article  CAS  PubMed  Google Scholar 

  13. 13

    Honma, T., Kawahata, S., Ishida, M., et al., Novel peptide toxins from the sea anemone Stichodactyla haddoni, Peptides, 2008, vol. 29, pp. 536−544.

    Article  CAS  PubMed  Google Scholar 

  14. 14

    Hrzenjak, T., Hrzenjak, M., Kasuba, V., et al., A new source of biologically active compounds—earthworm tissue (Eisenia foetida, Lumbruicus rubelus), Comp. Biochem. Physiol., 1992, vol. 102, pp. 441−447.

    Article  CAS  Google Scholar 

  15. 15

    Jouiaei, M., Yanagihara, A., and Madio, B., Ancient venom systems: a review on Cnidaria toxins, Toxins, 2015, vol. 7, pp. 2251−2271.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    Kauschke, E. and Mohrig, W., Cytotoxic activity in the coelomic fluid of the annelid Eisenia foetida, J. Comp. Physiol. B, 1987, vol. 157, pp. 77−83.

    Article  CAS  PubMed  Google Scholar 

  17. 17

    Kem, W., Anabaseine as a molecular model for design of Alpha7 nicotinic receptor agonist drugs, Perspectives in Molecular Toxinology, Ménez, A., Ed., Chichester, England: Wiley, 2002, pp. 297−314.

    Google Scholar 

  18. 18

    Kuzmenkov, A., Fedorova, I., Vassilevski, A., and Grishin, E., Cysteine-rich toxins from Lachesana tarabaevi spider venom with amphiphilic C-terminal segments, Biochim. Biophys. Acta, 2013, vol. 1828, no. 2, pp. 724−731.

    Article  CAS  PubMed  Google Scholar 

  19. 19

    Leary, S., Underwood, W., and Anthony, R., AVMA Guidelines for the Euthanasia of Animals: 2013 edition, Shaumburg, Ill.: Am. Vet. Med. Assoc., 2013, p. 67.

    Google Scholar 

  20. 20

    Lowry, O., Rosebrough, N., Farr, A., et al., Protein measurement with the Folin phenol reagent, J. Biol. Chem., 1951, vol. 193, pp. 265−275.

    CAS  PubMed  Google Scholar 

  21. 21

    Mariottini, G.L. and Pane, L., Mediterranean jellyfish venoms: a review on Scyphomedusae, Mar. Drugs, 2010, vol. 8, pp. 1122−1152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 22

    Masuda, A., Baba, T., Dohmae, N., et al., Mucin (qniumucin), a glycoprotein from jellyfish, and determination of its main chain structure, J. Nat. Prod., 2007, vol. 70, pp. 1089−1092.

    Article  CAS  PubMed  Google Scholar 

  23. 23

    Miyazawa, K., Higashiyama, M., Ito, K., et al., Tetrodotoxin in two species of ribbon worm (Nemertini), Lineus fuscoviridis and Tubulanus punctatus, Toxicon, 1988, vol. 26, pp. 867−874.

    Article  CAS  PubMed  Google Scholar 

  24. 24

    Morishige, H., Sugahara, T., Nishimoto, S., et al. Immunostimulatory effects of collagen from jellyfish in vivo, Cytotechnology, 2011, vol. 63, pp. 481−492.

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25

    Ohta, N., Sato, M., Ushida, K., et al., Jellyfish mucin may have potential disease-modifying effects on osteoarthritis, BMC Biotechnol., 2009, vol. 9, pp. 98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 26

    Popović, M., Grdiša, M., and Hrženjak, T., Glycolipoprotein G-90 obtained from the earthworm Eisenia foetida exerts antibacterial activity, Vet. Arh., 2005, vol. 75, no. 2, pp. 119−128.

    Google Scholar 

  27. 27

    Regier, J., Shultz, J., Ganley, A., et al., Resolving arthropod phylogeny: exploring phylogenetic signal within 41 kb of protein-coding nuclear gene sequence, Syst. Biol., 2008, vol. 57, pp. 920−938.

    Article  CAS  PubMed  Google Scholar 

  28. 28

    Romanenko, L., Uchino, M., Kalinovskaya, N., and Mikhailov, V., Isolation, phylogenetic analysis and screening of marine mollusc-associated bacteria for antimicrobial, hemolytic and surface activities, Microbiol. Res., 2008, vol. 163, pp. 633−644.

    Article  PubMed  Google Scholar 

  29. 29

    Shiomi, K., Honma, T., Idev M., et al., An epidermal growth factor-like toxin and two sodium channel toxins from the sea anemone Stichodactyla gigantean, Toxicon, 2003, vol. 41, pp. 229−236.

    Article  CAS  PubMed  Google Scholar 

  30. 30

    Silchenko, A.S., Kalinovsky, A.I., Avilov, S.A., et al., Triterpene glycosides from the sea cucumber Eupentacta fraudatrix. Structure and biological action of cucumariosides A1, A3, A4, A5, A6, A12 and A15, seven new minor non-sulfated tetraosides and unprecedented 25-keto,25-norholostane aglycone, Nat. Prod. Commun., 2012, vol. 7, no. 4, pp. 517−525.

    CAS  PubMed  Google Scholar 

  31. 31

    Sintsova, O., Gladkikh, I., Chausova, V., et al., Peptide fingerprinting of the sea anemone Heteractis magnifica mucus revealed neurotoxins, Kunitz-type proteinase inhibitors and a new β-defensin α-amylase inhibitor, J. Proteomics, 2018, vol. 173, pp. 12−21.

    Article  CAS  PubMed  Google Scholar 

  32. 32

    Stein, E. and Cooper, E., Carbohydrate and glycoprotein inhibitors of naturally occurring and induced agglutinins in the earthworm Lumbricus terrestris, Comp. Biochem. Physiol., 1983, vol. 76, pp. 197−206.

    Google Scholar 

  33. 33

    Uliasz, T.F. and Hewett, S.J., A microtiter trypan blue absorbance assay for the quantitative determination of excitotoxic neuronal injury in cell culture, J. Neurosci. Methods, 2000, vol. 100, pp. 157−163.

    Article  CAS  PubMed  Google Scholar 

  34. 34

    Wojdani, A., Stein, E., Alfred, L., and Cooper, E.L., Mitogenic effect of earthworm (Lumbricus terrestris) coelomic fluid on mouse and human lymphocytes, Immunobiology, 1984, vol. 166, pp. 157−167.

    Article  CAS  PubMed  Google Scholar 

  35. 35

    Zhuang, Y., Sun, L., and Li, B., Production of the angiotensin-I-converting enzyme (ACE)-inhibitory peptide from hydrolysates of jellyfish (Rhopilema esculentum) collagen, Food Bioproc. Technol., 2010, vol. 5, pp. 1622−1629.

    Article  CAS  Google Scholar 

  36. 36

    Zhuang, Y., Sun, L., Zhang Y., and Liu G., Antihypertensive effect of long-term oral administration of jellyfish (Rhopilema esculentum) collagen peptides on renovascular hypertension, Mar. Drugs, 2012, vol. 10, pp. 417−426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information



Corresponding author

Correspondence to E. V. Leychenko.

Additional information

Translated by I. Barsegova

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kozlovskii, S.A., Sintsova, O.V., Pislyagin, E.A. et al. The Biological Activity of Extracts of Marine Invertebrates from Troitsa Bay (Sea of Japan). Russ J Mar Biol 44, 465–470 (2018).

Download citation


  • invertebrates
  • Cnidaria
  • Annelida
  • Nemertea
  • Sipuncula
  • insectotoxins
  • biologically active compounds