The influence of сestodes parasitizing in the small intestine of herring gull chicks on the activity of the host proteases

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The activity of proteases and subclasses of proteases in small intestines of the herring gull (Larus argentatus (Pontoppidan, 1763)) chicks were determined. Changes of the protease activity in chicks infested by cestodes Tetrabothrius erostris (Loennberg, 1889) (Cestoda: Tetrabothriidae), Microsomacanthus ductilus (Linton, 1927) (Cestoda: Hymenolepididae), Wardium cirrosa (Krabbe, 1869) (Cestoda: Aploparaksidae), Arctotaenia tetrabothrioides (Loennberg, 1890) and Alcataenia larina (Krabbe, 1869) (Cestoda: Dilepididae) were studied. The activity of serine proteases decreased in the small intestine of gulls at the sites of cestode parasitism with high infestation values (M. ductilus in the proximal segment, W. cirrosa in the distal segment, A. tetrabothrioides, T. erostris and A. larina in the medial segment). The activity of cysteine proteases increased in the sites of localization of cestodes M. ductilus, W. cirrosa and A. larina. All the studied cestodes adsorbed proteases on the surface of the tegument, most of those were represented by serine proteases. Cestode homogenates of W. cirrosa, M. ductilus, A. tetrabothrioides, T. erostris and A. larina inhibited the activity of host proteases and the activity of commercial trypsin.

Full Text

Restricted Access

About the authors

M. M. Kuklina

Мурманский морской биологический институт РАН

Author for correspondence.
Email: MM_Kuklina@mail.ru
Russian Federation, Мурманск

V. V. Kuklin

Мурманский морской биологический институт РАН

Email: MM_Kuklina@mail.ru
Russian Federation, Мурманск

References

  1. Бондаренко С.К., Контримавичус В.Л. 2006. Аплопараксиды диких и домашних птиц. Основы цестодологии. М., Наука, 443 с. [Bondarenko S.K., Kontrimavichus V.L. 2006. Aploparaksidae of wild and domesticated birds. M., Nauka, 443 pp. (in Russian)].
  2. Извекова Г.И., Куклина М.М. 2014. Заражение цестодами и активность пищеварительных гидролаз позвоночных животных. Успехи современной биологии 134 (3): 304–315. [Izvekova G.I., Kuklina M.M. 2014. Infection by cestodes and activity of digestive enzymes in invertebrate hosts. Biological Bulletin Reviews 134 (3): 304–315. (in Russian)].
  3. Кузьмина В.В. 1976. Применение метода последовательной десорбции α-амилазы с отрезка кишки при изучении мембранного пищеварения у рыб. Вопр. ихтиологии 16 (5): С. 944–946. [Kuz´mina V.V. 1976. Application of the method of sequential desorption of α-amylase from an intestine segment in the study of membrane digestion in fish. Vopr. Ikhtiol. 16 (5): 944–946. (in Russian)].
  4. Куклин В.В., Кисова Н.Е. 2007. Гельминты чаек рода Larus Баренцева моря. Вест. Южного Научного Центра 3 (2): 64–71. [Kuklin V.V., Kisova H.E. 2007. Helminths of gulls of the genus Larus of the Barents Sea. Vest. YUzhnogo Nauchnogo Centra 3 (2): 64–71. (in Russian)].
  5. Куклина М.М. 2015. Биохимические показатели плазмы крови серебристой чайки при инвазии Tetrabothrius erostris (Cestoda: Tetrabothriidae). Российский паразитологический журнал 4: 79–84. [Kuklina M.M. 2015. Biochemical values of blood in herring gulls at invasion by Tetrabothrius erostris (Cestoda: Tetrabothriidae). Russian Journal of Parasitology 4: 79–84. (in Russian)]. https://doi: 10 12737/16664
  6. Куклина М.М., Куклин В.В. 2017. Wardium cirrosa (Cestoda: Aploparaksidae): локализация в кишечнике серебристой чайки и влияние на пищеварительную активность хозяина. Паразитология 51 (3): 213–223. [Kuklina M.M., Kuklin V.V. 2017. Wardium cirrosa (Cestoda: Aploparaksidae): localization in the intestine of the herring gull and impact on digestive activity of the host. Parazitologia 51 (3): 213–223. (in Russian)].
  7. Спасская Л.П., Спасский А.А. 1978. Цестоды птиц СССР. Т. 9. Дилепидиды лимнофильных птиц. М., Наука, 315 с. [Spasskaya L.P., Spasskii A.A. 1978. Cestodes of birds of the USSSR. V. 9. Dilepidids of limnophilic birds. M., Nauka, 315 pp. (in Russian)].
  8. Темирова С.И., Скрябин А.С. 1978. Основы цестодологии. Тетработриаты и мезоцистоидаты. М., Наука, 186 с. [Temirova S.I., Skryabin A.S. 1978. Fundamentals of cestodology. Tetrobothryates and mesocystoidates. M., Nauka, 186 pp. (in Russian)].
  9. Фролова Т.В., Извекова Г.И. 2018. Влияние заражения цестодой Proteocephalus torulosus Batsch, 1786 на активность ферментов в кишечнике синца (Ballerus ballerus L.). Паразитология 52 (4): 292–303. [Frolova T.V., Izvekova G.I. 2018. The influence of cestode infection with Proteocephalus torulosus Batsch, 1786 on the enzyme activity in the intestine of the zope (Ballerus ballerus L.). Parazitologia 52 (4): 292–303. (in Russian)]. https://doi: 10.7868/S0031184718040042
  10. Alarcón F.J., Martínez T.F., Barranco P., Cabello T., Díaz M., Moyano F.J. 2002. Digestive proteases during development of larvae of red palm weevil, Rhynchophorus errugineus (Olivier, 1790) (Coleoptera: Curculionidae). Insect Biochemistry and Molecular Biology 32: 265–274. https://doi.org/10.1016/s0965-1748(01)00087-x
  11. Dalton J.P., Skelly P., Halton D.W. 2004. Role of the tegument and gut in nutrient uptake by parasitic platyhelminths. Can. J. Zool. 82: 211–232. https://doi.org/10.1139/z03-213
  12. Frolova T.V., Izvekov E.I., Solovyev M.M., Izvekova G.I. 2019. Activity of proteolytic enzymes in the intestine of bream Abramis brama infected with cestodes Caryophyllaeus laticeps (Cestoda, Caryophyllidea). Comparative Biochemistry and Physiology, Part B 235: 38–45. https://doi.org/10.1016/j.cbpb.2019.05.009.
  13. Frolova T.V., Izvekova G.I. 2022. A comparative analysis of the effect of intestinal cestodes in different fish species on proteolytic enzyme activity. Journal of Evolutionary Biochemistry and Physiology 58 (3): 644–651. https://doi: 10.1134/S0022093022030024
  14. Frolova T.V., Izvekova G.I. 2023. Metabolic adaptation of fish intestinal helminthes: inhibitory ability towards proteases in cestodes Triaenophorus nodulosus. Journal of Evolutionary Biochemistry and Physiology 59 (5): 370–377. https://doi: 10.31857/S0044452923050042
  15. Izvekova G.I. 2013. Activity of digestive enzymes in burbots Lota lota (Linnaeus) depending on their infestation with Eubothrium rugosum (Batch) (Cestoda, Pseudophyllidea). Inland Water Biol. 6: 57–61. https://doi.org/10.1134/S1995082913010069
  16. Izvekova G.I., Solovyev M.M. 2016. Characteristics of the effect of cestodes parasitizing the fish intestine on the activity of the host proteinases. Biology Bulletin 43: 146–151. https://doi.org/10.1134/S1062359016010076
  17. Izvekova G.I., Frolova T.V., Izvekov E.I. 2017. Adsorption and inactivation of proteilytic enzymes by Triaenophorus nodulosus (Cestoda). Helminthologia 54(1): 3–10. https://doi: 10.1515/helm-2017-0001
  18. Kuklin V.V., Kuklina M.M. 2021. Age Dynamics of Helminth Fauna of the Herring Gull (Larus argentatus) in Kola Bay, Barents Sea. Biology Bulletin 48 (8): 1160–1169. https://doi: 10.1134/S1062359021080173
  19. Kuklina M.M., Kuklin V.V. 2006. Effect of helminthic infestation on the biochemical parameters of gulls of the genus Larus in the Barents Sea region. Doklady Biological Sciences 411 (1): 471–474. 10.1134/S0012496606060135' target='_blank'>https://doi: 10.1134/S0012496606060135
  20. Kuklina M.M., Kuklin V.V. 2011. Peculiarities of protein hydrolysis on the digestive transport surfaces of the intestine of the kittiwake Rissa tridactyla and Alcataenia larina (Cestoda, Dilepididae) parasitizing it. Biology Bulletin 38 (5): 470–475. https://doi: 10.1134/S1062359011050098
  21. Kuklina M.M., Kuklin V.V. 2016a. The activities of digestive enzymes as determinant factor in the localization of Tetrabothrius erostris (Cestoda: Tetrabothriidae) in the intestine of the herring gull Larus argentatus Pontoppidan. Inland Water Biology 9 (2): 189–195. https://doi: 10.134/S1995082916010107
  22. Kuklina M.M., Kuklin V.V. 2016b. Diphyllobothrium dendriticum (Cestoda: Diphyllobothriidae) in the intestinal tract of the herring gull Larus argentatus: localization and trophic parameters. Biology Bulletin 43 (4): 329–334. https://doi: 10.1134/S1062359016040063
  23. Kuklina M.M., Kuklin V.V. 2018. Effect of Cestodal Infestation on the Distribution Pattern of Digestive Enzyme Activities along the Small Intestine of the Kittiwake (Rissa tridactyla). Journal of Evolutionary Biochemistry and Physiology 54(4): 292–299. https://DOI: 10.1134/S0022093018040051
  24. Rogozhin E.A., Solovyev M.M., Frolova T.V., Izvekova G.I. 2019. Isolation and partial structural characterization of new Kunitz-type trypsin inhibitors from the pike cestode Triaenophorus nodulosus. Molecular & Biochemical Parasitology 233. https://doi.org/10.1016/j.molbiopara.2019.111217
  25. Ryzhikov K.M., Rusavy B., Khokhlova I.G., Tolkatchova L.M., Kornyuchin V.V. 1985. Helmints of Fish-Eating Birds of the Palaearctic Region II. Academia Publishing House, Czechoslovak Academy of Sciences, Prague, Czechoslovakia, 411 pp.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure 1. The proportion of serine proteases and metalloproteases in different fractions washed of cestode tegument M. ductilus, A. tetrabothrioides, T. erostris, A. larina и W. cirrosa (%). The proportion of serine proteases exceeded the proportion of metalloproteases (*the differences are significant relative to the values of the proportion of metalloproteases, p < 0.05). 1 – fraction Д1, 2 – fraction Д2, 3 – fraction Д3, 4 – fraction Д4

Download (164KB)
Indexing metadata
3. Figure 2. Effect of cestode homogenates and PMSF on the activity of commercial trypsin (0.01 mg/ml). The figure shows the proportion of inhibition of commercial trypsin activity by cestode and PMSF homogenates (%)

Download (79KB)
Indexing metadata
4. Figure 3. Effect of cestode homogenates and PMSF on the activity of proteases of the small intestine mucosa in herring gull chicks. The figure shows the proportion of inhibition of protease activity by cestode and PMSF homogenates (%). Cestode homogenates A. tetrabothrioides, T. erostris, A. larina and W. cirrosa had a higher inhibitory effect compared with PMSF (serine protease inhibitor) (*differences are significant relative to the values of the proportion of PMSF inhibition, p < 0.05)

Download (79KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences