Phenoloxidase and trypsin in germ-free larvae of Artemia fed with cooked unicellular diets: Examining the alimentary and protective effects of putative beneficial bacterium, yeast and microalgae against vibriosis

Journal of Experimental Marine Biology and Ecology

Volumn 381, Issue 2, 2009, Pages 90-97

  Rojas Garcia C R ^a   Sorgeloos, P ^a   Bossier, P ^a  

^a Faculty of Bioscience Engineering   (Belgium)

Author keywords

Artemia; Feeding; Innate immunity; Phenoloxidase; Trypsin; Vibrio; Yeast

Indexed keywords

ARTIFICIAL DIET; BACTERIAL DISEASE; BIOCHEMISTRY; COMMERCIAL SPECIES; DIGESTIVE SYSTEM; ENZYME ACTIVITY; FOOD QUALITY; GROWTH RESPONSE; IMMUNITY; INFECTIVITY; INNATE BEHAVIOR; LARVA; MICROALGA; SHRIMP CULTURE; SYMBIONT; YEAST;

ALGAE; ARTEMIA; BACTERIA (MICROORGANISMS); ROSEOBACTER; SACCHAROMYCES CEREVISIAE; TETRASELMIS; TETRASELMIS SUECICA; VIBRIO; VIBRIO PROTEOLYTICUS;

EID: 70350584810     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2009.08.001     Document Type: Article

References (63)

1. Adachi K., Hirata T., Nagai K., Fujisawa S., and Sakaguchi M. Effects of beta-1,3-glucan on the activation of prophenoloxidase cascade in Penaeus japonicus hemocyte. Fish. Sci. 65 (1999) 926-929
2. Ashida M., Ishizaki Y., and Iwahana H. Activation of prophenoloxidase by bacterial cell walls or β-l,3 glucans in plasma of the silkworm Bombyx mori. Biochem. Biophys. Res. Commun. 113 (1983) 562-568
3. Aspán A., and Söderhäll K. Purification of prophenoloxidase from crayfish blood cells, and its activation by an endogenous serine proteinase. Insect Biochem. 21 (1991) 363-373
4. Bachère E., Lorgeril J., Saulnier D., Janech M.G., and Gueguen Y. Identification of genes that are differentially expressed in hemocytes of the Pacific blue shrimp (Litopenaeus stylirostris) surviving an infection with Vibrio penaeicida. Physiol. Genomics 21 (2005) 174-183
5. Bajaj-Elliott M. Trypsin and host defense: a new role for an old enzyme. Gut 52 (2003) 166-167
6. Becker B., Lommerse J.P.M., Melkonian M., Kamerling J.P., and Vliegenthart J.F.G. The structure of an acidic trisaccharide component from a cell wall polysaccharide preparation of the green alga Tetraselmis striata Butcher. Carbohydr. Res. 267 (1995) 313-321
7. Birkbeck T.H., and McHenery J.G. Degradation of bacteria by Mytilus edulis. Mar. Biol. 72 (1982) 7-15
8. Bohn J.A., and BeMiller J.N. (1→3)-Beta-d-glucans as biological response modifiers: a review of structure functional activity relationships. Carbohydr. Polym. 28 (1995) 3-14
9. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of dye binding. Anal. Biochem. 72 (1976) 248-254
10. Chen C., Rowley A.F., and Ratcliffe N.A. Detection, purification by immunoaffinity chromatography and properties of β-1,3-glucan-specific lectins from the sera of several insect species. Insect Biochem. Mol. Biol. 28 (1998) 721-731
11. Coutteau P., Lavens P., and Sorgeloos P. Baker's yeast as a potential substitute for live algae in aquaculture diets: Artemia as a case study. J. World Aquac. Soc. 21 (1990) 1-8
12. Douillet P. In: Sorgeloos P., Bengston D.A., Decleir W., and Jaspers E. (Eds). Effect of bacteria on the nutrition of the brine shrimp Artemia fed on dried diets. Artemia Research and Its Applications vol. 3 (1987), Universa Press, Wetteren, Belgium 295-308
13. D'Souza F.M.L., and Kelly G.J. Effects of a diet of a nitrogen-limited alga (Tetraselmis suecica) on growth, survival and biochemical composition of tiger prawn (Penaeus semisulcatus) larvae. Aquaculture 181 (2000) 311-329
14. Erlanger B.F., Kokowsky N., and Cohen W. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 95 (1961) 271-278
15. Ghuysen J.M., and Strominger J.L. Structure of the cell wall of Staphylococcus aureus, strain Copenhagen: II. Separation and structure of disaccharides. Biochemistry 2 (1963) 1119-1125
16. Gorman M., and Paskewitz S.M. Serine proteinases as mediators of mosquito immune responses. Insect Biochem. Mol. Biol. 31 (2000) 257-262
17. Govind S., and Nehm R.H. Innate Immunity in fruit flies: a textbook example of genomic recycling. PLoS Biol. 276 (2004) 1065-1068
18. Harris R.P., Samain J.F., Moal J., Jezequel M., and Poulet S.A. Effects of algal diet on the digestive enzyme activity in Calanus helgolandicus. Mar. Biol. 90 (1986) 353-361
19. Hassett R.P., and Landry M.R. Effects of diet and starvation on digestive enzyme activity and feeding behavior of the marine copepod Calanus pacificus. J. Plankton Res. 12 (1990) 991-1010
20. Hauton C., and Smith V.J. In vitro cytotoxicity of crustacean immunostimulants for lobster (Homarus gammarus) granulocytes demonstrated using the neutral red uptake assay. Fish Shell. Immunol. 17 (2004) 65-73
21. Hung S.Y., and Boucias D.G. Phenoloxidase activity in hemolymph of näive and Beauveria bassiana-infected Spodoptera exigua larvae. J. Invertebr. Pathol. 67 (1996) 35-40
22. Ibarrola I., Navarro E., Iglesias J.I.P., and Urrutia M.B. Time-course of digestive-enzyme acclimation in the cockle Cerastoderma edule. Mar. Biol. 135 (1999) 47-56
23. Intriago P., and Jones D.A. Bacteria as food for Artemia. Aquaculture 113 (1993) 115-127
24. Johnson A., Hurwitz R., and Kretchmer A. Adaptation of at pancreatic amylase and chymotrypsinogen to changes in diet. J. Nutrition 107 (1977) 87-96
25. Jørgensen N.O.G., Stepanaukas R., Pedersen A.G.U., Hansen M., and Nybroe O. Occurrence and degradation of peptidoglycan in aquatic environments. FEMS Microbiol. Ecol. 46 (2003) 269-280
26. Karlsson C., Korayem A.M., Scherfer C., Dushay M.S., and Theopold U. Proteomic analysis of the Drosophila larval hemolymph clot. J. Biol. Chem. 279 (2004) 52033-52041
27. Kawabata S., and Iwanaga S. Role of lectins in the innate immunity of horseshoe crab. Dev. Comp. Immunol. 23 (1999) 391-400
28. Kulicke W.M., Lettau A.I., and Thielking H. Correlation between immunological activity, molar mass, and molecular structure of different (1→3)-β-d-glucans. Carbohydr. Res. 297 (1997) 135-143
29. Kumlu M., and Jones D.A. The effect of live and artificial diets on growth, survival, and trypsin activity in larvae of Penaeus indicus. J. World Aquac. Soc. 26 (1995) 406-415
30. Le Moullac G., and Haffner P. Environmental factors affecting immune responses in Crustacea. Aquaculture 191 (2000) 121-131
31. Le Moullac G., Klein B., Sellos D., and Van Wormhoudt A. Adaptation of trypsin, chymotrypsin and α-amylase to casein level and protein source in Penaeus vanammei (Crustacea Decapoda). J. Exp. Mar. Biol. Ecol. 208 (1996) 107-125
32. Le Moullac G., Soyez C., Saulnier D., Ansquer D., Avarre J.C., and Levy P. Effect of hypoxic stress on the immune response and the resistance to vibriosis of the shrimp Penaeus stylirostris. Fish Shell. Inmunol. 8 (1998) 621-629
33. Lewis L.D., and Williams J.A. Regulation of cholecystokinin secretion by food, hormones and neural pathways in the rat. Am. J. Physiol. 258 (1990) G512-G518
34. Lovett D.L., and Felder D.L. Ontogenetic change in digestive enzyme activity of larval and postlarval white shrimp Penaeus setiferus (Crustacea, Decapoda, Penaeidae). Biol. Bull. 178 (1990) 144-159
35. Ma C., and Kanost M.R. A β-1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J. Biol. Chem. 275 (2000) 7505-7514
36. Magnelli P., Cipollo J.F., and Abeijon C. A refined method for the determination of Saccharomyces cerevisiae cell wall composition and β-1,6-glucan fine structure. Anal. Biochem. 301 (2002) 136-150
37. Marques A., François J.-M., Dhont J., Bossier P., and Sorgeloos P. Influence of yeast quality on performance of gnotobiotically grown Artemia. J. Exp. Mar. Biol. Ecol. 310 (2004) 247-264
38. Martin G.G., Lin H.M.J., and Luc C. Reexamination of hemocytes in brine shrimp (Crustacea, Branchiopoda). J. Morphol. 242 (1999) 283-294
39. Misra C., Das B., Pradhan J., Pattnaik P., Sethi S., and Mukherjee S. Changes in lysosomal enzyme activity and protection against Vibrio infection in Macrobrachium rosenbergii (De Man) post larvae after bath immunostimulation with β-glucan. Fish Shell. Immunol. 17 (2004) 389-395
40. Mucklow P.T., Vizoso D.B., Jensen K.H., Refardt D., and Ebert D. Variation in phenoloxidase activity and its relation to parasite resistance within and between populations of Daphnia magna. Proc. R. Soc. Lond. B 271 (2004) 1175-1183
41. Mølck A.-M., Poulsen M., Christensen H.R., Lauridsen T.S., and Madsen C. Immunotoxicity of nucleic acid reduced BioProtein - a bacterial derived single cell protein - in Wistar rats. Toxicology 174 (2002) 183-200
42. Navarro J.M., Labarta U., Fernández-Reiriz M.J., and Velasco A. Feeding behavior and differential absorption of biochemical components by the infaunal bivalve Mulinia edulis and the epibenthic Mytilus chilensis in response to changes in food regimes. J. Exp. Mar. Biol. Ecol. 287 (2003) 13-35
43. Peters R., and Raftos D.A. The role of phenoloxidase suppression in QX disease outbreaks among Sydney rock oysters (Saccostrea glomerata). Aquaculture 223 (2003) 29-39
44. Richards E.H., and Edwards J.P. Parasitism of Lacanobia oleracea (Lepidoptera) by the ectoparasitoid, Eulophus pennicornis, is associated with a reduction in host haemolymph phenoloxidase activity. Comp. Biochem. Physiol B 127 (2000) 289-298
45. Rombaut G., Dhert P., Vanderberghe J., Verschuere L., Sorgeloos P., and Verstraete W. Selection of bacteria enhancing the growth of axenically hatched rotifers (Brachionus plicatilis). Aquaculture 176 (1999) 195-207
46. Sakai M. Current research status of fish immunostimulants. Aquaculture 172 (1999) 63-92
47. Samain J.F., Moal J., Daniel J.Y., Le Coz J.R., and Jezequel M. The digestive enzymes amylase and trypsin during the development of Artemia: effect of food conditions. In: Persoone G., Sorgeloos P., Roels O., and Jaspers R. (Eds). The Brine Shrimp Artemia. Physiology, Biochemistry, Molecular Biology vol. 2 (1980), Universa Press, Wetteren, Belgium 238-255 664 pp.
48. Samain J.F., Moal J., Daniel J.Y., and Le Coz J.R. Possible process of nutritive adaptations for zooplankton: a demonstration on Artemia. Kiel. Meeresforsch. 5 (1981) 218-228
49. Shelby K.S., Adeyeye O.A., Okot-Kotber B.M., and Webb B.A. Parasitism-linked block of host plasma melanization. J. Invertebr. Pathol. 75 (2000) 218-225
50. Sick L. Nutritional effect of five species of microalgae on the growth, development and survival of the brine shrimp Artemia salina. Mar. Biol. 35 (1976) 69-78
51. Smith V.J., and Söderhäll K. A comparison of phenoloxidase activity in the blood of marine invertebrates. Dev. Comp. Immunol. 15 (1991) 251-261
52. Söderhäll K., and Cerenius L. Role of the prophenoloxidase-activating system in invertebrate immunity. Curr. Opin. Immunol. 10 (1998) 23-28
53. Sorgeloos P., Bossuyt E., Laviña E., Baeza-Mesa M., and Persoone G. Decapsulation of Artemia cysts: a simple technique for the improvement of the use of brine shrimp in aquaculture. Aquaculture 12 (1977) 311-315
54. Sung H.H., Kou G.H., and Song Y.L. Vibriosis resistance induced by glucan treatment in tiger shrimp (Penaeus monodon). Fish Pathol. 29 (1994) 11-17
55. Ueberschär B. The use of tryptic enzyme activity measurement as a nutritional condition index laboratory calibration data and field applications. ICES Mar. Sci. Symp. 201 (1995) 119-129
56. Verschuere L., Rombaut G., Huys G., Dhont J., Sorgeloos P., and Verstraete W. Microbial control of the culture of Artemia juveniles through preemptive colonization by selected bacterial strains. Appl. Environ. Microbiol. 65 (1999) 2527-2533
57. Verschuere L., Heang H., Criel G., Sorgeloos P., and Verstraete W. Selected bacterial strains protect Artemia spp. from pathogenic effects of Vibrio proteolyticus CW8T2. Appl. Environ. Microbiol. 66 (2000) 1139-1146
58. Walne P.R. The food value of 13 species of unicellular algae to Artemia salina. ICES Fish. Improv. Comm. 5 (1967) 1-7
59. Wang S.H., and Chen J.C. The protective effect of chitin and chitosan against Vibrio alginolyticus in white shrimp Litopenaeus vannamei. Fish Shell. Immunol. 19 (2005) 191-204
60. Wang Y.C., Chang P.S., and Chen H.Y. Tissue distribution of prophenoloxidase transcript in the Pacific white shrimp Litopenaeus vannamei. Fish Shell. Immunol. 20 (2006) 414-418
61. Wilks S.A., and Sleigh M.A. Lectin binding sites on Euplotes mutabilis (Tuffrau, 1960) and the implications for food particle selection. Eur. J. Protistol. 40 (2004) 153-162
62. Yasuda K., and Taga N. A mass culture method for Artemia salina using bacteria as food. Mer 18 (1980) 53-62
63. Yu C., Lee A.M., Bassler L.B., and Roseman S. Chitin utilization by marine bacteria: a physiological function for bacterial adhesion to immobilized carbohydrates. J. Biol. Chem. 266 (1991) 24260-24267