Skip to main content
SpringerLink
Log in

Role of peptidases of the intestinal microflora and prey in temperature adaptations of the digestive system in planktivorous and benthivorous fish

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Many fish enzymatic systems possess limited adaptations to low temperature; however, little data are available to judge whether enzymes of fish prey and intestinal microbiota can mitigate this deficiency. In this study, the activity of serine peptidases (casein-lytic, mainly trypsin and hemoglobin-lytic, mainly chymotrypsin) of intestinal mucosa, chyme and intestinal microflora in four species of planktivorous (blue bream) and benthivorous (roach, crucian carp, perch) was investigated across a wide temperature range (0–70 °C) to identify adaptations to low temperature. At 0 °C, the relative activity of peptidases of intestinal mucosa (<13 %) and usually intestinal microflora (5–12.6 %) is considerably less than that of chyme peptidases (up to 40 % of maximal activity). The level of peptidase relative activity in crucian carp intestinal microflora was 45 % of maximal activity. The shape of t°-function curves of chyme peptidase also differs in fish from different biotopes. Fish from the littoral group are characterized by a higher degree of adaptation of chyme casein-lytic peptidases to functioning at low temperatures as compared to fish from the pelagic group. The role of intestinal microbiota and prey peptidases in digestive system adaptations of planktivorous and benthivorous fish to low temperatures is discussed.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anson M (1938) The estimation of pepsin, trypsin, papain and cathepsin with hemoglobin. J Gen Phys 22:79–83

    Article  CAS  Google Scholar 

  • Askarian F, Zhou Z, Olsen RE, Sperstad S, Ringo E (2012) 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. Aquac Res 326–329:1–8

    Article  Google Scholar 

  • Austin B (2006) The bacterial microflora of fish, revised. Sci World J 6:931–945

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Buddington RK, Weiher E (1999) The application of ecological principles and fermentable fibers to manage the gastrointestinal tract ecosystem. J Nutr 129:1446–1450

    Google Scholar 

  • Buddington RK, Krogdahl A, Bakke-Mckellep ÀÌ (1997) The intestines of carnivorous fish: structure and functions and relations with diet. Acta Physiol Scand. Suppl:67–80

  • Buddington RK, Williams CH, Nagata Y (2000) Fermentable fibers and the gastrointestinal tract bacteria: comparisons of fiber types and mouse strains. Microb Ecol Health Dis 12:225–232

    Article  Google Scholar 

  • Cahill MM (1990) Bacterial flora of fishes: a review. Microb Ecol 19:21–41

    Article  CAS  PubMed  Google Scholar 

  • Clements KD (1997) Fermentation and gastrointestinal microorganisms in fishes. In: Mackie RI, White BA (eds) Gastrointestinal ecosystems and fermentations. Chapman and Hall, New York, pp 156–198

    Google Scholar 

  • Dabrowski K (1979) The role of proteolytic enzymes in fish digestion. In: Cultivation of fish fry and its live food, vol 5. Eur Maricult Soc Bradine, Belgium. Special Publ., pp 107–126

  • Dabrowski K, Glogowski J (1977a) Studies on the proteolytic enzymes of invertebrates constituting fish food. Hydrobiologia (Hagua) 52:171–174

    Article  CAS  Google Scholar 

  • Dabrowski K, Glogowski J (1977b) The role of exogenic proteolytic enzymes in digestion processes in fish. Hydrobiologia (Hagua) 54:129–134

    Article  CAS  Google Scholar 

  • Dean RT (1980) Regulation and mechanisms of degradation of endogenous proteins by mammalian cells: general consideration. In: Wildenthal K (ed) Degradative processes in heart and skeletal muscle. Elsevier, North-Holland Biomed. Press, Amsterdam, pp 3–30

    Google Scholar 

  • Dixon M, Webb EC (1964) Enzymes, 2nd edn. Longmans, Green & Co., London, New York, p 950

    Google Scholar 

  • Esakkiraj P, Immanuel G, Sowmya SV, Iyapparaj P, Palavesam A (2009) Evaluation of protease-producing ability of fish gut isolate Bacillus cereus. Food Bioprocess Technol 2:383–390

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gelman AG, Kuz’mina VV, Drabkin V, Glatman M (2008) Temperature adaptations of fish digestive enzymes. In: Cyrino JEP, Bureau D, Kapoor BG (eds) Feeding and digestive functions in fishes. Science Publishers, Enfield, NH, pp 155–226

    Chapter  Google Scholar 

  • Gerking SD (1994) Feeding ecology of fish. Acad. Press, San-Diego

    Google Scholar 

  • Ghosh K, Sen SK, Ray AK (2002) Characterization of bacilli isolated from gut of rohu, Labelio rohita, finderlings and its significance in digestion. J Appl Aquac 12:33–42

    Article  Google Scholar 

  • Hamid A, Sakata T, Kakimoto D (1979) Microflora in the alimentary tract of gray mullet (4. Estimation of enzymic activities of the intestinal bacteria). Bull Jpn Soc Sci Fish 45(1):99–106

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN (1973) Strategies of biochemical adaptation. WB Saunders Company, Philadelphia, London, Toronto

    Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. University Press, Oxford, New York

    Google Scholar 

  • Hoshino T, Ishizaki K, Sakamoto T, Kumeta H, Yumoto I, Matsuyama H, Ohgiya S (1997) Isolation of a Pseudomonas species from fish intestine that produces a protease active at low temperature. Lett Appl Microbiol 25:70–72

    Article  CAS  PubMed  Google Scholar 

  • Izvekova GI, Plotnikov AO (2011) Hydrolytic activity of symbiotic microflora enzymes in pike (Esox lucius L.) intestines. Inland Water Biol 4(1):72–77

    Article  Google Scholar 

  • Kapahi P, Chen D, Rogers AN, Katewa SD (2010) With mTOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab 11:453–465

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kishimura H, Tokuda Y, Klomklao S, Benjakul S, Ando S (2006) Enzymatic characteristics of trypsin from pyloric ceca of spotted mackerel (Scomber australasicus). J Food Biochem 30:466–477

    Article  CAS  Google Scholar 

  • Kolkovsky S, Tandler A, Kissil GW, Gertler A (1993) The effect of dietary exogenous digestive enzymes on ingestion, assimilation, growth and survival of gilthead seabream (Sparus aurata, Sparidae, Linnaeus) larvae. Fish Physiol Biochem 12:203–209

    Article  Google Scholar 

  • Kurokawa T, Shiraishi M, Suzuki T (1998) Quantification of exogenous protease derived from zooplankton in the intestine of Japanese sardine (Sardinops melanotictus) larvae. Aquaculture 161:491–499

    Article  CAS  Google Scholar 

  • Kuz’mina VV (1985) Temperature adaptations of enzymes realizing membrane digestion in fresh-water teleosts. Zh Obshch Biol 46(6):824–837 (in Russian)

    Google Scholar 

  • Kuz’mina VV (1990) Effect of temperature on the level of total proteolytic activity of digestive tract in some species of fresh water teleosts. J Ichthyol 4(29):668–677

    Google Scholar 

  • Kuz’mina VV (1991) The peculiarities of the evolution of digestive–transportive functions in fish. J Evol Biochem Physiol 27(2):167–175 (in Russian)

    Google Scholar 

  • Kuz’mina VV (1999) Effect of temperature on the activity of some hydrolases in aquatic invertebrate. J Evol Biochem Physiol 35(1):15–19 (in Russian)

    Google Scholar 

  • Kuz’mina VV (2000) Contribution of induced autolysis to digestion processes in consumers of second order (hydrobionts as example). Rep Russ Acad Sci 339(1):172–174 (in Russian)

    Google Scholar 

  • Kuz’mina VV (2005) Physiological and biochemical principles of exotrothy processes in fish. Nauka Publ, Moscow (in Russian)

    Google Scholar 

  • Kuz’mina VV (2008) Classical and modern conceptions of fish digestion. In: Cyrino JEP, Bureau D, Kapoor BG (eds) Feeding and digestive functions in fishes. Science Publishers, Enfield, NH, pp 85–154

    Chapter  Google Scholar 

  • Kuz’mina VV, Golovanova IL (2004) Contribution of prey proteinases and carbohydrases in fish digestion. Aquaculture 234:347–360

    Article  Google Scholar 

  • Kuz’mina VV, Pervushina KA (2004) Effect of the temperature and pH on the activity of proteinases of intestinal mucosa and intestinal micro flora of fish. J Evol Biochem Physiol 40(3):214–219 (in Russian)

    Google Scholar 

  • Kuz’mina VV, Skvortsova EG (2002) Bacteria of alimentary canal and their role in fish digestive processes. Adv Curr Biol 122(6):569–579 (in Russian)

    Google Scholar 

  • Kuz’mina VV, Skvortsova EG, Shalygin MV (2012) Effect of temperature on the activity of proteinases of intestinal microbiota and intestinal mucosa of fishes of different ecological groups. J Evol Biochem Physiol 48(2):120–125 (in Russian)

    Google Scholar 

  • Kuz’mina VV, Gelman AG (1997) Membrane-linked digestion. Rev Fish Sci 5(2):99–129

    Article  Google Scholar 

  • Lauff M, Hofer R (1984) Proteolytic enzymes in fish development and the importance of dietary enzymes. Aquaculture 37(4):335–346

    Article  CAS  Google Scholar 

  • Lubianskienė V, Jastiuginienė R (1996) Antibiotic and fermentative activitiy of bacteria found in water and digestive tract of fish from lake Druksiai at Ignalina Nuclear Power Plant. Ekologija (Vilnius) 2:3–7

    Google Scholar 

  • Lubianskienė V, Verbikas Yu, Jankevicus K, Lasauskenė L, Gribauskenė V, Tryapshenė O, Iusolenenė U, Jastiuginenė R, Babyanskas M, Yanskauskenė R (1989) Obligate symbiosis of digestive tract microbiota and organism. Mokslas, Vilnius, 191 pp (in Russian)

  • Martinova EA (2012) Kinase mTOR and its role in the cellular response to the stress. Membr Cell Biol 6(1):9–19

    Google Scholar 

  • Mattheis Th (1964) Ökologie der bakterien in darm von sűsswassernuttfishen. Z Fisch 12:6–10

    Google Scholar 

  • Munilla-Moran R, Stark JR, Babour A (1990) The role of exogenous enzymes in digestion in cultured turbot larvae (Scophthalmus maximus L.). Aquaculture 88:337–350

    Article  CAS  Google Scholar 

  • Nemova NN (1978) Cathepsins of animal tissues. In: Sidorov VS (ed) Ecological and biological chemistry of animals. Karel. Sci. Center Akad. Sci. SSSR, Petrozavodsk, pp 76–88 (in Russian)

    Google Scholar 

  • Nikolskiy GV (1980) Structure of species and regularity of variability of fish. Pishch. Prom, Moskow, 184 pp (in Russian)

  • Oozeki Y, Bailey KM (1995) Ontogenetic development of digestive enzyme activities in larval walleye pollock, Theragra chalcogramma. Mar Biol 122(2):177–186

    CAS  Google Scholar 

  • Panin LE, Majanskaja NN (1987) Lysosomes: a role in adaptation and recovery. Nauka, Novosibirsk (in Russian)

    Google Scholar 

  • Pavlisko A, Rial A, de Vecchi S, Coppes Z (1997a) Properties of pepsin and trypsin isolated from the digestive tract of Parona signata “Palometa”. J Food Biochem 21:289–308

    Article  CAS  Google Scholar 

  • Pavlisko A, Rial A, Coppes Z (1997b) Characterization of trypsin purified from the pyloric caeca of the southwest Atlantic white croaker Micropogohias furnieri (Sciaenidae). J Food Biochem 21:383–400

    Article  Google Scholar 

  • Rawlings ND, Tolle DP, Barrett AJ (2004) MEROPS: the peptidase database. Nucleic Acids Res (Database issue) 32:D160–D164

    Article  CAS  Google Scholar 

  • Ray AK, Roy T, Mondal S, Ringo E (2010) Identification of gut associated amylase, cellulase and protease-producing bacteria in three species of Indian major carps. Aquac Res 41:1462–1469

    CAS  Google Scholar 

  • Richter-Otto W, Fehrmann M (1956) Zur methodik von darmflora untersuchungen. Ernährungsforsch 1:584–586

    Google Scholar 

  • Ringo E, Birkbeck TH (1999) Intestinal microflora of fish and fry: a review. Aquac Res 30(2):73–93

    Article  Google Scholar 

  • Ringø E, Sperstad S, Myklebust R, Refstie S, Krogdahl Å (2006) Characterisation of the microbiota associated with intestine of Atlantic cod (Gadus morhua L.): the effect of fish meal, standard soybean meal and a bioprocessed soybean meal. Aquaculture 261:829–841

    Article  Google Scholar 

  • Shcherbina MA, Pershina IF (1984) Intake and digestion of essential nutrients and energy of mixed fodder VBS-RZh in carp finderlings in the condition of the addition to it larvae of chironomids, vol 42. Tr. VNIIPRKh, Moskow, pp 46–54 (in Russian)

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

    Article  Google Scholar 

  • Šyvokieně J (1989) Symbiont digestion in hydrobionts and insects. Mokslas, Vilnius, 223 pp (in Russian)

  • Šyvokieně J, Mitzkeně L, Milereně E, Repechka R, Vaitonis G (1996) Microflora of digestive tract of Kaunas reservoir hydrobionts. Ekologija (Vilnius) 1:29–34

    Google Scholar 

  • Trust TJ, Sparrow RAH (1974) The bacterial flora in the alimentary tract of freshwater salmonid fishes. Can J Microbiol 20:1219–1228

    Article  CAS  PubMed  Google Scholar 

  • Trust TJ, Bull LM, Currie BR, Buckley JT (1979) Obligate anaerobic bacteria in the gastrointestinal microflora of the grass carp (Ctenopharingodon idella), goldfish (Carassius auratus), and rainbow trout (Salmo gairdneri). J Fish Res Board Can 36(10):1174–1179

    Article  Google Scholar 

  • Ugolev AM (1985) Evolution of digestion and principles of evolution of functions. Nauka, Leningrad (in Russian)

    Google Scholar 

  • Ugolev AM, Kuz’mina VV (1993a) Digestive processes and adaptations in fish. Gidrometeoizdat, Sanct-Petersburg (in Russian)

    Google Scholar 

  • Ugolev AM, Kuz’mina VV (1993b) Membrane hydrolases of fish enterocytes: temperature adaptation. Comp Biochem Physiol 106B(2):443–452

    CAS  Google Scholar 

Download references

Acknowledgments

This study was partly supported by the Russian Foundation for Basic Research, Project No. 13-04-00248.

Author information

Authors and Affiliations

  1. I.D.Papanin Institute for Biology of Inland Waters RAS, PO Box 152742, Borok, Yaroslavl, Russia

    V. V. Kuz’mina & M. V. Shalygin

  2. FSBEI HPE Yaroslavl State Agricultural Academy, PO Box 150042, Yaroslavl, Russia

    V. V. Kuz’mina, E. G. Skvortsova & M. V. Shalygin

  3. Natural Resources Research Institute, University of Minnesota Duluth, Miller Trunk Highway, PO Box 5013, Duluth, MN, USA

    K. E. Kovalenko

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

    You can also search for this author in PubMed Google Scholar

  2. E. G. Skvortsova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. V. Shalygin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. E. Kovalenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. V. Kuz’mina.

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., Skvortsova, E.G., Shalygin, M.V. et al. Role of peptidases of the intestinal microflora and prey in temperature adaptations of the digestive system in planktivorous and benthivorous fish. Fish Physiol Biochem 41, 1359–1368 (2015). https://doi.org/10.1007/s10695-015-0091-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-015-0091-4

Keywords

Search

Navigation