Inducible tolerance to dietary protease inhibitors in Daphnia magna

Journal of Experimental Biology

Volumn 215, Issue 12, 2012, Pages 2051-2059

  Von Elert, Eric ^a   Zitt, Anja ^b   Schwarzenberger, Anke ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Cyanobacteria; Daphnia; Tolerance

Indexed keywords

BACTERIAL TOXIN; CHYMOTRYPSIN; CYANOBACTERIAL TOXIN; MARINE TOXIN; MICROCYSTIN; PEPTIDE HYDROLASE; PROTEINASE INHIBITOR; TRYPSIN;

ANIMAL; ARTICLE; DAPHNIA; DIGESTION; ENZYMOLOGY; HERBIVORY; METABOLISM; MICROCYSTIS; PHYSIOLOGY; SCENEDESMUS;

ANIMALS; BACTERIAL TOXINS; CHYMOTRYPSIN; DAPHNIA; DIGESTION; HERBIVORY; MARINE TOXINS; MICROCYSTINS; MICROCYSTIS; PEPTIDE HYDROLASES; PROTEASE INHIBITORS; SCENEDESMUS; TRYPSIN;

EID: 84862532784     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.068742     Document Type: Article

References (55)

1. Agrawal, M. K., Bagchi, D. and Bagchi, S. N. (2001). Acute inhibition of protease and suppression of growth in zooplankter, Moina macrocopa, by Microcystis blooms collected in central India. Hydrobiologia 464, 37-44. (Pubitemid 34170079)
2. Agrawal, M. K., Zitt, A., Bagchi, D., Weckesser, J., Bagchi, S. N. and Von Elert, E. (2005). Characterization of proteases in guts of Daphnia magna and their inhibition by Microcystis aeruginosa PCC 7806. Environ. Toxicol. 20, 314-322. (Pubitemid 40827451)
3. Agrawal, M. K., Ghosh, S. K., Bagchi, D., Weckesser, J., Erhard, M. and Bagchi, S. N. (2006). Occurrence of microcystin-containing water blooms in central India. J. Microbiol. Biotechnol. 16, 212-218. (Pubitemid 43732594)
4. Baumann, H. I., Keller, S., Wolter, F. E., Nicholson, G. J., Jung, G., Susmuth, R. D. and Jüttner, F. (2007). Planktocyclin, a cyclooctapeptide protease inhibitor produced by the freshwater cyanobacterium Planktothrix rubescens. J. Nat. Prod. 70, 1611-1615. (Pubitemid 350155412)
5. Beynon, R. J. and Bond, J. S. (2001). Proteolytic Enzymes: a Practical Approach, 2nd edn. Oxford: Oxford University Press.
6. Bister, B., Keller, S., Baumann, H., Nicholson, G., Weist, S., Jung, G., Süssmuth, R. D. and Jüttner, F. (2004). Cyanopeptolin 963A, a chymotrypsin inhibitor of Microcystis PCC 7806. J. Nat. Prod. 67, 1755-1757. (Pubitemid 39426139)
7. Blom, J. F., Bister, B., Bischoff, D., Nicholson, G., Jung, G., Süssmuth, R. D. and Jüttner, F. (2003). Oscillapeptin J, a new grazer toxin of the freshwater cyanobacterium Planktothrix rubescens. J. Nat. Prod. 66, 431-434. (Pubitemid 36384027)
8. Blom, J. F., Baumann, H. I., Codd, G. A. and Jüttner, F. (2006). Sensitivity and adaptation of aquatic organisms to oscillapeptin J and [D-Asp(3),(E)-Dhb(7)]microcystin-RR. Arch. Hydrobiol. 167, 547-559. (Pubitemid 44606813)
9. Brandl, M. and Massnig, U. (2003). Vesicular phospholipid gels. In Liposomes (ed. V. P. Torchilin and V. Weissig), pp. 353-372. Oxford: Oxford University Press.
10. Carmichael, W. W. (1994). The toxins of cyanobacteria. Sci. Am. 270, 64-72.
11. Carpenter, S. R. and Kitchell, J. F. (1984). Plankton community structure and limnetic primary production. Am. Nat. 124, 159-172. (Pubitemid 15276758)
12. Christoffersen, K., Riemann, B., Klysner, A. and Sondergaard, M. (1993). Potential role of fish predation and natural-populations of zooplankton in structuring a plankton community in eutrophic lake water. Limnol. Oceanogr. 38, 561-573.
13. De Bernardi, R. and Giussani, G. (1990). Are blue-green algae a suitable food for zooplankton? An overview. Hydrobiologia 200/201, 29-41.
14. Gademann, K. and Portmann, C. (2008). Secondary metabolites from cyanobacteria: complex structures and powerful bioactivities. Curr. Org. Chem. 12, 326-341.
15. Glawe, G. A., Zavala, J. A., Kessler, A., Van Dam, N. M. and Baldwin, I. T. (2003). Ecological costs and benefits correlated with trypsin protease inhibitor production in Nicotiana attenuata. Ecology 84, 79-90. (Pubitemid 36892990)
16. Gustafsson, S. and Hansson, L. A. (2004). Development of tolerance against toxic cyanobacteria in Daphnia. Aquat. Ecol. 38, 37-44. (Pubitemid 38463714)
17. Gustafsson, S., Rengefors, K. and Hansson, L. A. (2005). Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects. Ecology 86, 2561-2567. (Pubitemid 41408052)
18. Hairston, N. G., Lampert, W., Cáceres, C. E., Holtmeier, C. L., Weider, L. J., Gaedke, U., Fischer, J. M., Fox, J. A. and Post, D. M. (1999). Lake ecosystems: rapid evolution revealed by dormant eggs. Nature 401, 446.
19. Hansson, L. A., Gustafsson, S., Rengefors, K. and Bomark, L. (2007). Cyanobacterial chemical warfare affects zooplankton community composition. Freshw. Biol. 52, 1290-1301. (Pubitemid 46872699)
20. Jähnichen, S., Petzoldt, T. and Benndorf, J. (2001). Evidence for control of microcystin dynamics in Bautzen reservoir (Germany) by cyanobacterial population growth rates and dissolved inorganic carbon. Arch. Hydrobiol. 150, 177-196. (Pubitemid 32139736)
21. Jongsma, M. A. and Bolter, C. (1997). The adaptation of insects to plant protease inhibitors. J. Insect Physiol. 43, 885-895. (Pubitemid 27521869)
22. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
23. Lampert, W. (1987). Feeding and nutrition in Daphnia. In Daphnia, Vol. 45, Memorie dell'Instituto Italiano di Idrobiologia dott. Marco de Marchi (ed. R. H. Peters and R. de Bernadi), pp. 143-192. Verbania Pallanza: Consiglio Nazionale delle Richerche Instituto Italiano di Idrobiologia.
24. Lampert, W. and Rothhaupt, K. O. (1991). Alternating dynamics of rotifers and Daphnia magna in a shallow lake. Arch. Hydrobiol. 120, 447-456.
25. Lampert, W., Rothhaupt, K. O. and Von Elert, E. (1994). Chemical induction of colony formation in a green alga (Scenedesmus acutus) by grazers (Daphnia). Limnol. Oceanogr. 39, 1543-1550. (Pubitemid 26447871)
26. 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. (Pubitemid 37538072)
27. Lürling, M. and Van der Grinten, E. (2003). Life-history characteristics of Daphnia exposed to dissolved microcystin-LR and to the cyanobacterium Microcystis aeruginosa with and without microcystins. Environ. Toxicol. Chem. 22, 1281-1287. (Pubitemid 37092482)
28. Martin-Creuzburg, D., Von Elert, E. and Hoffmann, K. H. (2008). Nutritional constraints at the cyanobacteria-Daphnia interface: the role of essential lipids. Limnol. Oceanogr. 53, 456-468. (Pubitemid 351705399)
29. McQueen, D. J., Post, J. R. and Mills, E. L. (1986). Trophic relationship in freshwater pelagic ecosystems. Can. J. Fish. Aquat. Sci. 43, 1571-1581.
30. McQueen, D. J., Johannes, M. R. S., Post, J. R., Stewart, T. J. and Lean, D. R. S. (1989). Bottom-up and top-down impacts on fresh-water pelagic community structure. Ecol. Monogr. 59, 289-309. (Pubitemid 20420542)
31. Paerl, H. W. and Huisman, J. (2008). Blooms like it hot. Science 320, 57-58.
32. Paterson, M. J., Findlay, D. L., Salki, A. G., Hendzel, L. L. and Hesslein, R. H. (2002). The effects of Daphnia on nutrient stoichiometry and filamentous cyanobacteria: a mesocosm experiment in a eutrophic lake. Freshw. Biol. 47, 1217-1233. (Pubitemid 34791927)
33. Porter, K. G. and McDonough, R. (1984). The energetic cost of response to bluegreen algal filaments by cladocerans. Limnol. Oceanogr. 29, 365-369.
34. Rohrlack, T., Chrisoffersen, K., Hansen, P. E., Zhang, W., Czarnecki, O., Henning, M., Fastner, J., Erhard, M., Neilan, B. A. and Kaebernick M. (2003). Isolation, characterization, and quantitative analysis of microviridin J, a new Microcystis metabolite toxic to Daphnia. J. Chem. Ecol. 29, 1757-1770. (Pubitemid 36988563)
35. Rohrlack, T., Christoffersen, K., Kaebernick, M. and Neilan, B. A. (2004). Cyanobacterial protease inhibitor microviridin J causes a lethal molting disruption in Daphnia pulicaria. Appl. Environ. Microbiol. 70, 5047-5050. (Pubitemid 39095539)
36. Rohrlack, T., Christoffersen, K., Dittmann, E., Nogueira, I., Vasconcelos, V. and Borner, T. (2005a). Ingestion of microcystins by Daphnia: intestinal uptake and toxic effects. Limnol. Oceanogr. 50, 440-448. (Pubitemid 40428470)
37. Rohrlack, T., Christoffersen, K. and Friberg-Jensen, U. (2005b). Frequency of inhibitors of daphnid trypsin in the widely distributed cyanobacterial genus Planktothrix. Environ. Microbiol. 7, 1667-1669. (Pubitemid 41345908)
38. Sano, T. and Kaya, K. (1995). Oscillamide Y, a chymotrypsin inhibitor from toxic Oscillatoria agardhii. Tetrahedron Lett. 36, 5933-5936.
39. Sano, T. and Kaya, K. (1996). Oscillatorin, a chymotrypsin inhibitor from toxic Oscillatoria agardhii. Tetrahedron Lett. 37, 6873-6876. (Pubitemid 26293457)
40. Sarnelle, O. (2007). Initial conditions mediate the interaction between Daphnia and bloom-forming cyanobacteria. Limnol. Oceanogr. 52, 2120-2127. (Pubitemid 47612135)
41. Sarnelle, O. and Wilson, A. E. (2005). Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnol. Oceanogr. 50, 1565-1570. (Pubitemid 41356437)
42. Sarnelle, O., Gustafsson, S. and Hansson, L. A. (2010). Effects of cyanobacteria on fitness components of the herbivore Daphnia. J. Plankton Res. 32, 471-477.
43. Schwarzenberger, A., Zitt, A., Kroth, P., Mueller, S. and Von Elert, E. (2010). Gene expression and activity of digestive proteases in Daphnia: effects of cyanobacterial protease inhibitors. BMC Physiol. 10, 6.
44. Tonk, L., Welker, M., Huisman, J. and Visser, P. M. (2009). Production of cyanopeptolins, anabaenopeptins, and microcystins by the harmful cyanobacteria Anabaena 90 and Microcystis PCC 7806. Harmful Algae 8, 219-224.
45. Van de Waal, D. B., Verspagen, J. M. H., Lurling, M., Van Donk, E., Visser, P. M. and Huisman, J. (2009). The ecological stoichiometry of toxins produced by harmful cyanobacteria: an experimental test of the carbon-nutrient balance hypothesis. Ecol. Lett. 12, 1326-1335.
46. Von Elert, E. (2002). Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnol. Oceanogr. 47, 1764-1773. (Pubitemid 36016834)
47. Von Elert, E. and Jüttner, F. (1997). Phosphorus limitation not light controls the exudation of allelopathic compounds by Trichormus doliolum. Limnol. Oceanogr. 42, 1796-1802. (Pubitemid 127687996)
48. Von Elert, E., Martin-Creuzburg, D. and Le Coz, J. R. (2003). Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proc. R. Soc. Lond. B 270, 1209-1214. (Pubitemid 36683467)
49. Von Elert, E., Agrawal, M. K., Gebauer, C., Jaensch, H., Bauer, U. and Zitt, A. (2004). Protease activity in guts of Daphnia magna: evidence for trypsin and chymotrypsin enzymes. Comp. Biochem. Physiol. 137B, 287-296. (Pubitemid 38429741)
50. Von Elert, E., Oberer, L., Merkel, P., Huhn, T. and Blom, J. F. (2005). Cyanopeptolin 954, a novel chlorine-containing chymotrypsin-inhibitor of Microcystis aeruginosa NIVA Cya43. J. Nat. Prod. 68, 1324-1327. (Pubitemid 41499423)
51. Weckesser, J., Martin, C. and Jakobi, C. (1996). Cyanopeptolins, depsipeptides from cyanobacteria. Syst. Appl. Microbiol. 19, 133-138. (Pubitemid 26280197)
52. Wilson, A. E. and Hay, M. E. (2007). A direct test of cyanobacterial chemical defense: variable effects of microcystin-treated food on two Daphnia pulicaria clones. Limnol. Oceanogr. 52, 1467-1479. (Pubitemid 47121559)
53. Wilson, A. E., Sarnelle, O. and Tillmanns, A. R. (2006). Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: metaanalysis of laboratory experiments. Limnol. Oceanogr. 51, 1915-1924. (Pubitemid 44185742)
54. Zavala, J. A., Patankar, A. G., Gase, K., Hui, D. Q. and Baldwin, I. T. (2004). Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol. 134, 1181-1190. (Pubitemid 38403225)
55. Zhu-Salzman, K., Koiwa, H., Salzman, R. A., Shade, R. E. and Ahn, J. E. (2003). Cowpea bruchid Callosobruchus maculatus uses a three-component strategy to overcome a plant defensive cysteine protease inhibitor. Insect Mol. Biol. 12, 135-145. (Pubitemid 36400264)