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Fisheries Science

, Volume 82, Issue 5, pp 835–841 | Cite as

Cellulolytic activity in the hepatopancreas of Chionoecetes opilio and Chionoecetes japonicus: enzymatic adaptations to deep sea environment

  • Kohsuke AdachiEmail author
  • Kento Tanimura
  • Toshiyuki Mitsui
  • Takami Morita
  • Ikuko Yosho
  • Kou Ikejima
  • Katsuji Morioka
Original Article Chemistry and Biochemistry
  • 219 Downloads

Abstract

Chionoecetes opilio and Chionoecetes japonicus are closely related crab species that inhabit bathymetrically distinct habitats. C. opilio is caught mainly in waters shallower than 500 m, whereas C. japonicus largely resides at depths below 500 m. In this study, the activity of partially purified cellulase (β-1,4-glucanase) from the hepatopancreas of C. opilio (CoCel) and C. japonicus (CjCel) was investigated under high static pressure. SDS-PAGE-zymogram analysis revealed a major band in both species, with a calculated molecular mass of 41 kDa. In tests under various static pressures from 0.1 to 200 MPa, CoCel maintained 80 % of its activity up to 20 MPa, but activity decreased sharply to 20 % at 200 MPa in a pressure-dependent manner. In contrast, CjCel was less sensitive to high pressure, and maintained 65 % activity at 200 MPa. The activity of both CoCel and CjCel followed Michaelis–Menten kinetics at normal pressure levels; however, enzymatic activity of both CoCel and CjCel was suppressed in a non-competitive manner. These results suggest that CjCel, which can maintain normal activity under extremely high static pressure, have become highly adapted to the deep sea environment compared with CoCel.

Keywords

Chionoecetes opilio Chionoecetes japonicus Cellulase Adaptation Deep sea Hydrostatic pressure 

Notes

Acknowledgments

The authors would like to thank Professor Fumiyoshi Abe (Department of Chemistry and Biological Science, College of Science and Engineering, Aoyama Gakuin University) for his useful advice. The authors are grateful to Hideaki Yamada from the Tottori Fisheries Experimental Station for kindly providing the experimental samples for preliminary study. This work was supported in part by the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research (JSPS KAKENHI; Grant Number 26520308).

Supplementary material

12562_2016_1014_MOESM1_ESM.pptx (45 kb)
Supplementary material 1 (PPTX 45 kb)

References

  1. 1.
    Yosho I, Hayashi I (1994) The bathymetric distribution of Chionoecetes opilio and C. japonicus (Majidae: Brachyura) in the western and northern areas of the Sea of Japan. Bull Jpn Sea Natl Fish Res Inst 44:59–71Google Scholar
  2. 2.
    Gibbs AG (1997) Biochemistry at depth. In: Randall DJ, Farrell AP (eds) Deep-sea fishes. Academic Press, London, pp 239–277CrossRefGoogle Scholar
  3. 3.
    Somero GN (2003) Protein adaptation to temperature and pressure: complementary roles of adaptive changes in amino acid sequence and internal milieu. Comp Biochem Physiol B 136:577–591CrossRefPubMedGoogle Scholar
  4. 4.
    Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632CrossRefPubMedGoogle Scholar
  5. 5.
    Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331CrossRefPubMedGoogle Scholar
  6. 6.
    Smant G, Stokkermans JP, Yan Y, de Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA 95:4906–4911CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Sugimura M, Watanabe H, Lo N, Saito H (2003) Purification, characterization, cDNA cloning and nucleotide sequencing of a cellulase from the yellow-spotted longicorn beetle, Psacothea hilaris. Eur J Biochem 270:3455–3460CrossRefPubMedGoogle Scholar
  8. 8.
    Byrne KA, Lehnert SA, Johnson SE, Moore SS (1999) Isolation of a cDNA encoding a putative cellulase in the red claw crayfish Cherax quadricarinatus. Gene 239:317–324CrossRefPubMedGoogle Scholar
  9. 9.
    Nishida Y, Suzuki K, Kumagai Y, Tanaka H, Inoue A, Ojima T (2007) Isolation and primary structure of a cellulase from the Japanese sea urchin Strongylocentrotus nudus. Biochimie 89:1002–1011CrossRefPubMedGoogle Scholar
  10. 10.
    Suzuki K, Ojima T, Nishita K (2003) Purification and cDNA cloning of a cellulase from abalone Haliotis discus hannai. Eur J Biochem 270:771–778CrossRefPubMedGoogle Scholar
  11. 11.
    Sakamoto K, Touhata K, Yamashita M, Kasai A, Toyohara H (2007) Cellulose digestion by common Japanese freshwater clam Corbicula japonica. Fish Sci 73:675–683CrossRefGoogle Scholar
  12. 12.
    Niiyama T, Toyohara H (2011) Widespread distribution of cellulase and hemicellulase activities among aquatic invertebrates. Fish Sci 77:649–655CrossRefGoogle Scholar
  13. 13.
    Kobayashi H, Hatada Y, Tsubouchi T, Nagahama T, Takami H (2012) The hadal amphipod Hirondellea gigas possessing a unique cellulase for digesting wooden debris buried in the deepest seafloor. PLoS One 7:e42727CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Adachi K, Toriyama K, Azekura T, Morioka K, Tongnunui K, Ikejima K (2012) Potent cellulase activity in the hepatopancreas of mangrove crabs. Fish Sci 78:1309–1314CrossRefGoogle Scholar
  15. 15.
    Jue C, Lipke P (1985) Determination of reducing sugars in the nanomole range with tetrazolium blue. J Biochem Biophys Methods 11:109–115CrossRefPubMedGoogle Scholar
  16. 16.
    Ohmae E, Gekko K, Kato C (2015) Environmental adaptation of dihydrofolate reductase from deep-sea bacteria. In: Akasaka K, Matsuki H (eds) High pressure bioscience—basic concepts, applications and frontiers. Springer, Berlin, pp 423–442Google Scholar
  17. 17.
    Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMedGoogle Scholar
  18. 18.
    Wong PT, Heremans K (1988) Pressure effects on protein secondary structure and hydrogen deuterium exchange in chymotrypsinogen: a Fourier transform infrared spectroscopic study. Biochim Biophys Acta 956:1–9CrossRefPubMedGoogle Scholar
  19. 19.
    Murakami C, Ohmae E, Tate S, Gekko K, Nakasone K, Kato C (2011) Comparative study on dihydrofolate reductases from Shewanella species living in deep-sea and ambient atmospheric-pressure environments. Extremophiles 15:165–175CrossRefPubMedGoogle Scholar
  20. 20.
    Silva JL, Foguel D, Royer CA (2001) Pressure provides new insights into protein folding, dynamics and structure. Trends Biochem Sci 26:612–618CrossRefPubMedGoogle Scholar
  21. 21.
    Eisenmenger MJ, Reyes-De-Corcuera JI (2009) High pressure enhancement of enzymes: a review. Enzym Microb Technol 45:331–347CrossRefGoogle Scholar
  22. 22.
    Ohmae E, Miyashita Y, Kato C (2013) Thermodynamic and functional characteristics of deep-sea enzymes revealed by pressure effects. Extremophiles 17:701–709CrossRefPubMedGoogle Scholar
  23. 23.
    Kawaida S, Kimura T, Toyohara H (2013) Habitat segregation of two dotillid crabs Scopimera globosa and Ilyoplax pusilla in relation to their cellulase activity on a marsh-dominated estuarine tidal flat in central Japan. J Exp Mar Biol Ecol 449:93–99CrossRefGoogle Scholar
  24. 24.
    Linton SM, Shirley AJ (2011) Isozymes from the herbivorous gecarcinid land crab, Gecarcoidea natalis that possess both lichenase and endo-β-1,4-glucanase activity. Comp Biochem Physiol B 160:44–53CrossRefPubMedGoogle Scholar
  25. 25.
    Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238CrossRefPubMedGoogle Scholar
  26. 26.
    Yasuda T (1967) Feeding habit of the zuwaigani, Chionoecetes opilio elongatus, in Wakasa Bay-I: specific composition of the stomach contents. Nippon Suisan Gakkaishi 33:315–319CrossRefGoogle Scholar
  27. 27.
    Yosho I (2009) Studies on biology and stock management of Beni-zuwai crab, Chionoecetes japonicus Rathbun, in the Sea of Japan. PhD dissertation, Tohoku University, Sendai, JapanGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2016

Authors and Affiliations

  • Kohsuke Adachi
    • 1
    Email author
  • Kento Tanimura
    • 1
  • Toshiyuki Mitsui
    • 2
  • Takami Morita
    • 3
  • Ikuko Yosho
    • 4
  • Kou Ikejima
    • 1
  • Katsuji Morioka
    • 1
  1. 1.Laboratory of Aquatic Product Utilization, Graduate School of AgricultureKochi UniversityKochiJapan
  2. 2.Aoyama-Gakuin UniversitySagamiharaJapan
  3. 3.National Research Institute of Fisheries ScienceYokohamaJapan
  4. 4.Japan Sea National Fisheries Research InstituteFisheries Research Agency JapanNiigataJapan

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