Characterization of proteases in guts of Daphnia magna and their inhibition by Microcystis aeruginosa PCC 7806

Environmental Toxicology

Volumn 20, Issue 3, 2005, Pages 314-322

  Agrawal, Manish K ^a,b,c   Zitt, Anja ^b   Bagchi, Divya ^a   Weckesser, Jürgen ^c   Bagchi, Suvendra N ^a   Von Elert, Eric ^b  

^a RANI DURGAVATI UNIVERSITY   (India)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Chymotrypsin; Cyanobacteria; Daphnia; Inhibition; Inhibitor; Microcystin; Microcystis; Peptide; Protease; Trypsin

Indexed keywords

BACTERIA; CHARACTERIZATION; ENZYME INHIBITION; FRACTIONATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; POLYPEPTIDES; SUBSTRATES; TOXICITY;

DAPHNIA MAGNA; PROTEASE INHIBITORS; PROTEASES; SYNTHETIC INHIBITORS; TRYPSINS;

ENZYMES;

CHYMOTRYPSIN; CYANOGINOSIN; PEPTIDE; PROTEINASE; PROTEINASE INHIBITOR; TRYPSIN;

CYANOBACTERIUM; DIGESTIVE SYSTEM; INHIBITION;

BACTERIAL STRAIN; CONFERENCE PAPER; CONTROLLED STUDY; DAPHNIA; ENZYME ANALYSIS; ENZYME SPECIFICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INTESTINE; MICROCYSTIS AERUGINOSA; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEINASE INHIBITION;

ANIMALS; BACTERIAL TOXINS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHYMOTRYPSIN; DAPHNIA; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME INHIBITORS; MICROCYSTIS; PEPTIDE HYDROLASES; PROTEINS; TRYPSIN;

BOVINAE; CYANOBACTERIA; DAPHNIA; DAPHNIA MAGNA; MAMMALIA; MICROCYSTIS; MICROCYSTIS AERUGINOSA; MICROCYSTIS AERUGINOSA PCC 7806;

EID: 16244417837     PISSN: 15204081     EISSN: None     Source Type: Journal    
DOI: 10.1002/tox.20123     Document Type: Conference Paper

References (47)

1. Agrawal MK, Bagchi D, Bagchi SN. 2001. Acute inhibition of protease and suppression of growth in zooplankter, Moina macrocopa, by Microcystis blooms collected in central India. Hydrobiologia 464:37-44.
2. Asgeirsson B, Leth-Larsen R, Thorolfsson M, Nedertoft MM, Hojrup P. 1998. The third serine proteinase with chymotrypsin specificity isolated from Atlantic cod (Gadus morhua) is a type-II elastase. Eur J Biochem 255:638-646.
3. Banker R, Carmeli S. 1999. Inhibitors of serine proteases from a waterbloom of the cyanobacterium Microcystis sp. Tetrahedron 55:10835-10844.
4. Benndorf J, Henning M. 1989. Daphnia and toxic blooms of Microcystis aeruginosa in Bautzen reservoir (GDR). Int Rev Hydrobiol 74:3-18.
5. Beynon RJ, Bond JS. 2001. Proteolytic enzymes: a practical approach. Oxford, UK: University Press. 340 p.
6. Bieth J, Spiess B, Wermuth CG. 1974. The synthesis and analytical use of a highly sensitive and convenient substrate of elastase. Biochem Med 11:350-357.
7. Blom JF, Bister B, Bischoff D, Nicholson G, Jung G, Süssmuth RD, Jüttner F. 2003. Oscillapeptin J, a new grazer toxin of the freshwater cyanobacterium Planktothrix rubescens. J Nat Prod 66:431-434.
8. Bonjouklian R, Smitka TA, Hunt AH, Occolowitz JL, Perun TJ, Doolin L, Stevenson S, Knauss L, Wijayaratne R, Szewczyk S, Patterson GML. 1996. A90720a, a serine-protease inhibitor isolated from a terrestrial blue-green-alga Microchaete loktakensis. Tetrahedron 52:395-404.
9. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
10. De Bernardi R, Giussani G. 1990. Are blue-green algae a suitable food for zooplankton? An overview. Hydrobiologia 200/ 2 01:29-41.
11. Delmer EG, Largman C, Brodrick JW, Geokas MC. 1979. A sensitive new substrate for chymotrypsin. Anal Biochem 99:316-320.
12. DeMott WR, Zhang QX, Carmichael WW. 1991. Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol Oceanogr 36 :1346-1357.
13. DeMott WR, Dhawale S. 1995. Inhibition of in-vitro protein phosphatase-activity in three zooplankton species by microcystin-LR, a toxin from cyanobacteria. Arch Hydrobiol 134:417-424.
14. Diaz M, Moyano FJ, García-Carreño FL, Alarcon FJ, Sarasquete MC. 1997. Substrate-SDS-PAGE determination of protease activity through larval development in sea bream. Aquacult Int 5:461-471.
15. Dittmann E, Neilan BA, Erhard M, Von Döhren H, Börner T. 1997. Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol Microbiol 26:779-787.
16. Erlanger BF, Kokowski N, Cohen W. 1961. The preparation and properties of two new chromogenic substrates of trypsin. Arch Biochem Biophys 95:271-278.
17. Fastner J, Erhard M, Von Döhren H. 2001. Determination of oligopeptide diversity within a natural population of Microcystis spp. (cyanobacteria) by typing single colonies by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Appl Environ Microb 67:5069-5076.
18. Gliwicz ZM, Lampert W. 1990. Food thresholds in Daphnia species in the absence and presence of blue-green filaments. Ecology 71:691-702.
19. Haney JF, Forsyth DJ, James MR. 1994. Inhibition of zooplankton filtering rates by dissolved inhibitors produced by natural occurring cyanobacteria. Arch Hydrobiol 132:1-13.
20. Ishida K, Matsuda H, Murakami M. 1998. Micropeptins 88-A to 88-F, chymotrypsin inhibitors from the cyanobacterium Microcystis aeruginosa (NIES-88). Tetrahedron 54:5545-5556.
21. Jungmann D. 1992. Toxic compounds isolated from Microcystis PCC 7806 that are more active against Daphnia than two microcystins. Limnol Oceanogr 37:1777-1783.
22. Jungmann D, Benndorf J. 1994. Toxicity to Daphnia of a compound extracted from laboratory and natural Microcystis spp, and the role of microcystins. Freshwater Biol 32:13-20.
23. Kirk KL, Gilbert JJ. 1992. Variation in herbivore response to chemical defenses: zooplankton foraging on toxic cyanobacteria. Ecology 73:2208-2218.
24. Kodani S, Suzuki S, Ishida K, Murakami M. 1999. Five new cyanobacterial peptides from water bloom materials of Lake Teganuma (Japan). FEMS Microbiol Lett 178:343-348.
25. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Lampert W. 1981. Inhibitory and toxic effects of blue-green algae on Daphnia. Int Rev Hydrobiol 66:285-298.
27. Landsberg JH. 2002. The effects of harmful algal blooms on aquatic organisms. Rev Fish Sci 10:113-390.
28. Lürling M. 2003. Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus. Limnol Oceanogr 48:2214-2220.
29. MacKintosh C, Beattie KA, Klumpp S, Cohen P, Codd GA. 1990. Cyanobacterial microcystin-LR is a potent and specific inhibitor of protein phosphatases 1 and 2A from both mammals and higher plants. FEBS Lett 264:187-192.
30. Martin C, Oberer L, Ino T, Koenig WA, Busch M, Weckesser J. 1993. Cyanopeptolins, new depsipeptides from the cyanobacterium Microcystis sp. PCC 7806. Journal of Antibiotics 46:1550-1556.
31. Martin-Creuzburg D, Von Elert E. 2004. Impact of ten dietary sterols on growth and reproduction of Daphnia galeata. J Chem Ecol 30:483-499.
32. Murakami M, Okita Y, Matsuda H, Okino T, Yamaguchi K. 1994. Aeruginosin 298-a, a thrombin and trypsin-inhibitor from the blue-green-alga Microcystis aeruginosa (NIES-298). Tetrahedron Lett 35:3129-3313.
33. Namikoshi M, Rinehart KL. 1996. Bioactive compounds produced by cyanobacteria. J Ind Microbiol Biot 17:373-384.
34. Nizan S, Dimentman C, Shilo M. 1986. Acute toxic effects of the cyanobacterium Microcystis aeruginosa on Daphnia magna. Limnol Oceanogr 29:935-949.
35. Pflugmacher S, Wiegand C, Oberemm A, Beattie KA, Krause E, Codd GA, Steinberg CEW. 1998. Identification of an enzymatically formed glutathione conjugate of the cyanobacterial hepatotoxin microcystin-LR: The first step of detoxification. Biochim Biophys Act 1425:527-533.
36. Porter KG, McDonough R. 1984. The energetic cost of response to blue-green algal filaments by cladocerans. Limnol Oceanogr 29:365-369.
37. Rohrlack T, Dittmann E, Henning M, Börner T, Kohl J. 1999. Role of microcystins in poisoning and food ingestion inhibition of Daphnia galeata caused by the cyanobacterium Microcystis aeruginosa. Appl Env Microbiol 65:737-739.
38. Rohrlack T, Dittmann E, Börner T, Christoffersen K. 2001. Effects of cell-bound microcystins on survival and feeding of Daphnia spp. Appl Env Microbiol 67:3523-3529.
39. Rohrlack T, Christoffersen K, Hansen PE, Zhang W, Czarnecki O, Henning M, Fastner J, Erhard M, Neilan BA, Kaebernick M. 2003. Isolation, characterization, and quantitative analysis of microviridin J, a new Microcystis metabolite toxic to Daphnia. J Chem Ecol 29:1757-1770.
40. Rohrlack T, Christoffersen K, Kaebernick M, Neilan BA. 2004. Microviridin J, a cyanobacterial protease inhibitor that causes a lethal molting disruption in Daphnia. Appl Env Microbiol 70:5047-5050.
41. Thostrup L, Christoffersen K. 1999. Accumulation of microcystin in Daphnia magna feeding on toxic Microcystis. Arch Hydrobiol 145:447-467.
42. Tsai IH, Lu PJ, Chuang JL. 1991. The midgut chymotrypsins of shrimps Penaeus monodon, Penaeus japonicus and Penaeus penicillatus. Biochim Biophys Act 1080:59-67.
43. Von Elert E, Wolffrom T. 2001. Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnol Oceanogr 46:1552-1558.
44. Von Elert E, Martin-Creuzburg D, Le Coz JR. 2003. Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proc R Soc B 270:1209-1214.
45. Von Elert E, Agrawal MK, Gebauer C, Jaensch H, Bauer U, Zitt A. 2004. Protease activity in guts of Daphnia magna: Evidence for trypsin and chymotrypsin enzymes. Comp Biochem Phys B 137:287-296.
46. Weckesser J, Martin C, Jakobi C. 1996. Cyanopeptolins, depsipeptides from cyanobacteria. Syst Appl Microbiol 19:133-138.
47. Yokokawa F, Inaizumi A, Shioiri T. 2001. Synthetic studies of micropeptin T-20, a novel 3-amino-6-hydroxy-2-piperidone (Ahp)-containing cyclic depsipeptide. Tetrahedron Lett 42:5903-5908.