Skip to main content
SpringerLink
Log in

Effect of pH on the proteinase activities in the intestine mucosa, chyme, and enteral microbiota in the piscivorous fish differing in their ecological traits

  • Published:
Journal of Ichthyology Aims and scope Submit manuscript

Abstract

The effect of pH on the activity of proteinases of intestine mucosa, chyme, and enteral microbiota was studied in three piscivorous fish species of the Rybinsk Reservoir differing in their ecological traits: pike Esox lucius, burbot Lota lota, and zander Sander lucioperca. In all fish species, studied pH of ten is optimal for the functioning of proteinases of intestine mucosa; in chyme proteinases, optimal pH values vary from six to ten. Optimal pH for functioning of proteinases of enteral microbiota is seven for zander and pike; pH of nine, for burbot. High activity of chyme and microbiota proteinases within the diapason of pH values of six to nine is a characteristic of burbot. Relative activity of proteinases of intestine mucosa in all fish species is not more than 15% of the maximal activity; that of chyme and enteral microbiota is lower than 40% in zander, close to 50% in burbot, and 80 and 50%, respectively, in pike. It is suggested that diversity of the patterns of pH-dependence of enteral microbiota proteinases relates to the specificity of microbiota in various ecological zones of the reservoir (littoral, sublittoral, and bathyal).

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anson, M., The estimation of pepsin, trypsin, papain, and cathepsin with hemoglobin, J. Gen. Physiol., 1938, vol. 22, pp. 79–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Askarian, F., Zhou, Z., Olsen, R.E., et al., Culturable autochthonous bacteria in Atlantic salmon (Salmo salar L.) fed diets with or without chitin. Characterization by 16S rRNA gene sequencing, ability to produce enzymes and in vitro growth inhibition of four fish pathogens, Aquaculture, 2012, vols. 326–329, pp. 1–8.

    Article  Google Scholar 

  • Barrington, E.J.W., The alimentary canal and digestion, in Physiology of Fishes, New York: Academic, 1957, vol. 1, pp. 109–161.

    Article  Google Scholar 

  • Belchior, S.G.E. and Vacca, G., Fish protein hydrolysis by a psychrotrophic marine bacterium isolated from the gut of hake (Merluccius hubbsi hubbsi), Can. J. Microbiol., 2006, vol. 52, pp. 1266–1271.

    Article  CAS  PubMed  Google Scholar 

  • Bogatyrenko, E.A., Characteristics of cultivated microbial heterotrophs from intestine of Far Eastern sea cucumber Apostichopus japonicus, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Vladivostok: Far Eastern Fed. Univ., 2013.

    Google Scholar 

  • Buddington, R.K., Krogdahl, A., and Bakke-Mckellep, A.M., The intestines of carnivorous fish: structure and functions and relations with diet, Acta Physiol. Scand., 1997, suppl. 638, pp. 67–80.

    CAS  Google Scholar 

  • Castillo-Yánez, F.J., Pacheco-Aguilar, R., García-Carreno, F.L., and Navarrete-Del Toro, M., Isolation and characterization of trypsin from pyloric caeca of Monterey sardine (Sardinops sagax caeruleus), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2005, vol. 140, pp. 91–98.

    Article  Google Scholar 

  • Esakkiraj, P., Immanuel, G., Sowmya, S.V., et al., Evaluation of protease-producing ability of fish gut isolate Bacillus cereus, Food Bioprocess Technol., 2009, vol. 2, pp. 383–390.

    Article  Google Scholar 

  • Ganguly, S. and Prasad, A. Microflora in fish digestive tract plays significant role in digestion and metabolism, Rev. Fish Biol. Fish., 2012, vol. 22, pp. 11–16.

    Article  Google Scholar 

  • Ghosh, K., Sen, S.K., and Ray, A.K., Characterization of bacilli isolated from gut of rohu, Labelio rohita, finderlings and its significance in digestion, J. Appl. Aquacult., 2002, vol. 12, pp. 33–42.

    Article  Google Scholar 

  • Hamid, A., Sakata, T., and Kakimoto, D., Microflora in the alimentary tract of grey mullet. Estimation of enzymic activities of the intestinal bacteria, Bull. Jpn. Soc. Sci. Fish., 1979, vol. 45, pp. 99–106.

    Article  CAS  Google Scholar 

  • Heu, M.S., Kim, H.R., and Pyeun, J.H., Comparison of trypsin and chymotrypsin from the viscera of anchovy, Engraulis japonica, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1995, vol. 112, pp. 557–567.

    Article  CAS  Google Scholar 

  • Hidalgo, M.C., Urea, E., and Sanz, A., Comparative study of digestive enzymes in fish with different nutritional habits. Proteolytic and amylase activities, Aquaculture, 1999, vol. 170, pp. 267–283.

    Article  CAS  Google Scholar 

  • Hjelmeland, K. and Raa, J., Characterization of trypsin type isozymes isolated from the arctic fish capelin (Mallotus villisus), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1982, vol. 71, pp. 557–562.

    Article  CAS  Google Scholar 

  • Hoshino, T., Ishizaki, K., Sakamoto, T., et al., Isolation of Pseudomonas species from fish intestine that produces a protease active at low temperature, Lett. Appl. Microbiol., 1997, vol. 25, pp. 70–72.

    Article  CAS  PubMed  Google Scholar 

  • Jónás, E., Rágyanszki, M., Oláh, J., and Boross, L., Proteolytic digestive enzymes of carnivorous (Silurus glanis L.), herbivorous (Hypophthlmichthys molitrix Val.) and omnivorous (Cyprinus carpio L.) fishes, Aquaculture, 1983, vol. 30, pp. 145–154.

    Article  Google Scholar 

  • Khablyuk, V.V., Purification and properties of digestive enzymes from hepatopancreas of a carp, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Krasnodar: Krasnodar. Polytech. Inst., 1984.

    Google Scholar 

  • Kishimura, H., Hayashi, K., Miyashita, Y., and Nonami, Y., Characteristics of two trypsin isozymes from the viscera of Japanese anchovy (Engraulis japonica), J. Food Biochem., 2005, vol. 29, pp. 459–469.

    Article  CAS  Google Scholar 

  • Kishimura, H., Klomklao, S., Benjakul, S., and Chun, B.-S., Characteristics of trypsin from the pyloric ceca of walleye pollock (Theragra chalcogramma), Food Chem., 2008, vol. 106, pp. 194–199.

    Article  CAS  Google Scholar 

  • Kolkovski, S., Tandler, A., Kissil, G.W., and Gertler, A., The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth, and survival of gilthead sea bream (Sparus aurata, Sparidae, Linnaeus) larvae, Fish Physiol. Biochem., 1993, vol. 12, pp. 203–209.

    Article  CAS  PubMed  Google Scholar 

  • Kolkovski, S., Tandler, A., and Izquierdo, M.S., Effects of live food, dietary digestive enzymes on the efficiency of microdiets for seabass Dicentrarchus labrax larvae, Aquaculture, 1997, vol. 148, pp. 313–322.

    Article  CAS  Google Scholar 

  • Kopylov, A.I. and Kosolapov, D.B., Mikrobnaya “petlya” v planktonnykh soobshchestvakh morskikh i presnovodnykh ekosistem (Microbial “Loop” in Planktonic Communities of Marine and Freshwater Ecosystems), Izhevsk: Knigo-Grad, 2011.

    Google Scholar 

  • Kumar, S., Garcia-Carreno, F.L., Chakrabarti, R., et al., Digestive proteases of three carps Catla catla, Labeo rohita and Hypophthalmichthys molitrix: partial characterization and protein hydrolysis efficiency, Aquacult. Nutr., 2007, vol. 13, pp. 381–388.

    Article  CAS  Google Scholar 

  • Kuz’mina, V.V., Contribution of induced autolysis to digestion in secondary consumers (exemplified by hydrobionts), Dokl. Biol. Sci., 2000, vol. 373, nos. 1–6, pp. 379–381.

    PubMed  Google Scholar 

  • Kuz’mina, V.V., Fiziologo-biokhimicheskie osnovy ekzotrofii ryb (Physiological and Biochemical Principles of Exotrophy Processes in Fish), Moscow: Nauka, 2005.

    Google Scholar 

  • Kuz’mina, V.V., Classical and modern conceptions of fish digestion, in Feeding and Digestive Functions in Fishes, Cyrino, J.E.P., et al., Eds., Enfield, NH: Sci. Publ., 2008, pp. 85–154.

    Chapter  Google Scholar 

  • Kuz’mina, V.V. and Nevalennyi, A.N., Influence of concentration of hydrogen ions on activity of carbohydrases from digestive tract of fishes, Vopr. Ikhtiol., 1983, vol. 23, no. 3, pp. 481–490.

    Google Scholar 

  • Kuz’mina, V.V. and Skvortsova, E.G., Bacteria of digestive tract and their role in digestion of fishes, Usp. Sovrem. Biol., 2002, vol. 122, no. 6, pp. 569–579.

    Google Scholar 

  • Kuz’mina, V.V., Skvortsova, E.G., Zolotareva, G.V., and Sheptitskiy, V.A., Influence of pH upon the activity of glycosidases and proteinases of intestinal mucosa, chime, and microbiota in fish, Fish Physiol. Biochem., 2011, vol. 37, no. 3, pp. 345–357.

    Article  PubMed  Google Scholar 

  • Kuz’mina, V.V., Zolotareva, G.V., and Sheptitskii, V.A., Effect of habitat conditions on proteinase and glycosidase activities in the gut microbiota of crucian carp in a wide range of pH, Russ. J. Ecol., 2014a, vol. 45, no. 4, pp. 303–309.

    Article  Google Scholar 

  • Kuz’mina, V.V., Zolotareva, G.V., and Sheptitskiy, V.A., Effect of pH on the activity of proteinases in intestinal mucosa, chyme, and microbiota of fish from the Cuciurgan reservoir, J. Ichthyol., 2014b, vol. 54, no. 8, pp. 591–597.

    Article  Google Scholar 

  • Kuz’mina, V.V., Zolotareva, G.V., and Sheptitskiy, V.A., Proteinase activity in food objects and associated microbial biota in fishes-ichthyophages in the wide range of pH, Probl. Biol. Produkt. Zhivotn., 2015, no. 1, pp. 42–52.

    Google Scholar 

  • Lubyanskene, V., Virbitskas, Yu., Yankyavichus, K., et al., Obligatnyi simbioz mikroflory pishchevaritel’nogo trakta i organizma (Obligate Symbiosis of Digestive Microflora and Organism), Vilnius: Mokslas, 1989.

    Google Scholar 

  • Mattheis, T., Das Vorkommen von Vibrio anguillarum in Ostseefischen, Z. Fish. N.F., 1964, vol. 12, pp. 259–263.

    Google Scholar 

  • Murakami, K. and Noda, M., Studies on proteinases from the digestive organs of sardine. I. Purification and characterization of three alkaline proteinases from the pyloric caeca, Biochim. Biophys. Acta, 1981, vol. 658, pp. 17–26.

    Article  CAS  PubMed  Google Scholar 

  • Nevalennyi, A.N., Bednyakov, D.A., and Novitskii, V.Yu., Complex analysis of specific membrane digestion in starry sturgeon, Vestn. Astrakh. Gos. Tekh. Univ., Ser. Rybn. Khoz., 2011, no. 2, pp. 93–98.

    Google Scholar 

  • Poddubnyi, A.G., Ekologicheskaya topografiya populyatsii ryb v vodokhranilishchakh (Ecological Topography of Fish Population in Reservoirs), Leningrad: Nauka, 1971.

    Google Scholar 

  • Ray, A.K., Ghosh, K., and Ringø, E., Enzyme-producing bacteria isolated from fish gut: a review, Aquacult. Nutr., 2012, vol. 18, no. 5, pp. 465–492.

    Article  CAS  Google Scholar 

  • Richter-Otto, W. and Fehrmann, M., Zur methodik von darmflora untersuchungen, Ernährungsforsch, 1956, vol. 1, no. 3, pp. 584–586.

    Google Scholar 

  • Shivokene, Ya.S., Simbiontnoe pishchevarenie u gidrobiontov i nasekomykh (Symbiotic Digestion of Hydrobionts and Insects), Vilnius: Mokslas, 1989.

    Google Scholar 

  • Skrodenyte-Arbaciauskiene, V., Proteolytic activity of the roach (Rutilus rutilus) intestinal microflora, Acta Zool. Litu., 2000, vol. 10, pp. 69–77.

    Article  Google Scholar 

  • Solovyev, M.M., Kashinskaya, E.N., Izvekova, G.I., and Glupov, V.V., pH values and activity of digestive enzymes in the gastrointestinal tract of fish in Lake Chany (West Siberia), J. Ichthyol., 2015, vol. 55, no. 2, pp. 251–258.

    Article  Google Scholar 

  • Torrissen, K.R., Characterization of proteases in the digestive tract of Atlantic salmon (Salmo salar) in comparison with rainbow trout (Salmo gairdneri), Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1984, vol. 77, pp. 669–674.

    Article  Google Scholar 

  • Ugolev, A.M. and Kuz’mina, V.V., Pishchevaritel’nye protsessy i adaptatsii u ryb (Digestive Processes and Adaptations in Fishes), St. Petersburg: Nauka, 1993.

    Google Scholar 

  • Zolotareva, G.V., Kuz’mina, V.V., and Sheptitskiy, V.A., Proteinase activity in food and associated microbial biota of fishes–benthophages in the wide range of pH, Probl. Biol. Produkt. Zhivotn., 2015, no. 1, pp. 61–69.

    Google Scholar 

  • Zozulya, L.V., Purification and properties of digestive enzymes of the silver carp, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Rostov-on-Don: Rostov State Univ., 1996.

    Google Scholar 

  • Zubkova, L.A., Bacterial flora of organs and tissues of the common carp (Cyprinus carpio L.), Tr. Kasp. Nauchno-Issled. Inst. Rybn. Khoz., 1965, vol. 20, pp. 117–121.

    Google Scholar 

  • Zubkova, L.A., Normal microbial flora of Volga zander (Lucioperca lucioperca), Tr. Kasp. Nauchno-Issled. Inst. Rybn. Khoz., 1966, vol. 22, pp. 81–85.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Papanin Institute of the Biology of Inland Waters, Russian Academy of Sciences (IBIW), Borok, Yaroslavl oblast, 152742, Russia

    V. V. Kuz’mina

  2. Shevchenko Transnistria State University (PSU), ul. 25 Oktyabrya 128, Tiraspol, MD-3300, Moldova

    G. V. Zolotareva & V. A. Sheptitskii

Authors
  1. V. V. Kuz’mina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. V. Zolotareva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. A. Sheptitskii
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. V. Kuz’mina.

Additional information

Original Russian Text © V.V. Kuz’mina, G.V. Zolotareva, V.A. Sheptitskii, 2016, published in Voprosy Ikhtiologii, 2016, Vol. 56, No. 1, pp. 102–108.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kuz’mina, V.V., Zolotareva, G.V. & Sheptitskii, V.A. Effect of pH on the proteinase activities in the intestine mucosa, chyme, and enteral microbiota in the piscivorous fish differing in their ecological traits. J. Ichthyol. 56, 147–153 (2016). https://doi.org/10.1134/S0032945216010070

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0032945216010070

Keywords

Search

Navigation