Molecular mechanisms of tolerance to cyanobacterial protease inhibitors revealed by clonal differences in Daphnia magna

Molecular Ecology

Volumn 21, Issue 19, 2012, Pages 4898-4911

  Schwarzenberger, Anke ^a   Kuster, Christian J ^a   Von Elert, Eric ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

adaptation; cyanobacterial protease inhibitors; Daphnia; Microcystis aeruginosa PCC 7806; molecular mechanisms; qPCR; tolerance

Indexed keywords

CHYMOTRYPSIN; TRYPSIN; TRYPSIN INHIBITOR;

ANIMAL; ARTICLE; CHEMISTRY; CYANOBACTERIUM; DAPHNIA; ENZYMOLOGY; FOOD CHAIN; GENETICS; GENOTYPE; GREEN ALGA; GROWTH, DEVELOPMENT AND AGING; IC 50; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY;

ANIMALS; CHLOROPHYTA; CHYMOTRYPSIN; CYANOBACTERIA; DAPHNIA; FOOD CHAIN; GENOTYPE; INHIBITORY CONCENTRATION 50; MOLECULAR SEQUENCE DATA; PHYLOGENY; TRYPSIN; TRYPSIN INHIBITORS;

CYANOBACTERIA; DAPHNIA; DAPHNIA MAGNA; DAPHNIIDAE; MICROCYSTIS AERUGINOSA; MICROCYSTIS AERUGINOSA PCC 7806;

EID: 84867097582     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05753.x     Document Type: Article

References (69)

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. (Pubitemid 34170079)
2. Agrawal MK, Zitt A, Bagchi D, et al,. (2005) Characterization of proteases in guts of Daphnia magna and their inhibition by Microcystis aeruginosa PCC 7806. Environmental Toxicology, 20, 314-322. (Pubitemid 40827451)
3. Blom JF, Baumann H, Codd GA, Jüttner F, (2006) Sensitivity and adaptation of aquatic organisms to oscillapeptin J and [D-Asp3,(E)-Dhb7] microcystin-RR. Archiv fuer Hydrobiologie, 167, 547-559. (Pubitemid 44606813)
4. Brito LO, Lopes AR, Parra JRP, Terra WR, Silva-Filho MC, (2001) Adaptation of tobacco budworm Heliothis virescens to proteinase inhibitors may be mediated by the synthesis of new proteinases. Comparative Biochemistry and Physiology B- Biochemistry and Molecular Biology, 128, 365-375. (Pubitemid 32157524)
5. Bustin SA, Benes V, Garson JA, et al,. (2009) The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55, 611-622.
6. Carmichael WW, (1992) Cyanobacteria secondary metabolites: the cyanotoxins. Journal of Applied Bacteriology, 72, 445-459.
7. Carmichael WW, (1994) The toxins of cyanobacteria. Scientific American, 270, 64-72.
8. Colbourne JK, (2005) wFleaBase: the Daphnia genome database. BMC Bioinformatics, 6, 45.
9. Colbourne JK, Pfrender ME, Gilbert D, et al,. (2011) The ecoresponsive genome of Daphnia pulex. Science, 331, 555-561.
10. Conant GC, Wolfe KH, (2008) Turning a hobby into a job: how duplicated genes find new functions. Nature Reviews Genetics, 9, 938-950. (Pubitemid 352719432)
11. Decaestecker E, Gaba S, Raeymaekers JAM, et al,. (2007) Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature, 450, 870-873. (Pubitemid 350231319)
12. DeMott WR, (1999) Foraging strategies and growth inhibition in five daphnids feeding on mixtures of a toxic cyanobacterium and a green alga. Freshwater Biology, 42, 263-274.
13. DeMott WR, Gulati RD, Van Donk E, (2001) Daphnia food limitation in three hypereutrophic Dutch lakes: evidence for exclusion of large-bodied species by interfering filaments of cyanobacteria. Limnology and Oceanography, 46, 2054-2060. (Pubitemid 34009954)
14. Dittmann E, Neilan BA, Erhard M, Von Doehren H, Börner T, (1997) Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Molecular Microbiology, 26, 779-787. (Pubitemid 27489339)
15. Downing JA, Watson SB, McCauley E, (2001) Predicting Cyanobacteria dominance in lakes. Canadian Journal of Fisheries and Aquatic Sciences, 58, 1905-1908. (Pubitemid 33023417)
16. Dybdahl MF, Storfer A, (2003) Parasite local adaptation: Red Queen versus Suicide King. Trends in Ecology and Evolution, 18, 523-530. (Pubitemid 37143679)
17. Ebert D, (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science, 265, 1084-1086. (Pubitemid 24293073)
18. Ebert D, (2008) Host-parasite coevolution: insights from the Daphnia-parasite model system. Current Opinion in Microbiology, 11, 290-301.
19. Gademann K, Portmann C, (2008) Secondary metabolites from cyanobacteria: complex structures and powerful bioactivities. Current Organic Chemistry, 12, 326-341.
20. Ghadouani A, Pinel-Alloul B, Prepas EE, (2003) Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities. Freshwater Biology, 48, 363-381. (Pubitemid 36174907)
21. Gilbert JJ, (1990) Differential effects of Anabaena affinis on cladocerans and rotifers: mechanisms and implications. Ecology, 71, 1727-1740.
22. Girard C, Le Metayer M, Bonade-Bottino M, Pham-Delegue MH, Jouanin L, (1998) High level of resistance to proteinase inhibitors may be conferred by proteolytic cleavage in beetle larvae. Insect Biochemistry and Molecular Biology, 28, 229-237. (Pubitemid 28313400)
23. Gustafsson S, (2007) Zooplankton Response to Cyanotoxins. Ph.D. thesis, Lund University.
24. Gustafsson S, Hansson LA, (2004) Development of tolerance against toxic cyanobacteria in Daphnia. Aquatic Ecology, 38, 37-44. (Pubitemid 38463714)
25. Hairston NG, Lampert W, Cáceres CE, et al,. (1999) Rapid evolution revealed by dormant eggs. Nature, 401, 446.
26. Hairston NG, Holtmeier CL, Lampert W, et al,. (2001) Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution, 55, 2203-2214. (Pubitemid 34045553)
27. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuclic Acids Symposium Series, 41, 95-98.
28. Hansson LA, Gustafsson S, Rengefors K, Bomark L, (2007) Cyanoabacterial chemical warfare affects zooplankton community composition. Freshwater Biology, 52, 1290-1301. (Pubitemid 46872699)
29. Hartl M, Giri AP, Kaur H, Baldwin IT, (2011) The multiple functions of plant serine protease inhibitors: defense against herbivores and beyond. Plant Signaling and Behavior, 6, 1009-1011.
30. Hawkins P, Lampert W, (1989) The effect of Daphnia body size on filtering rate inhibition in the presence of a filamentous cyanobacterium. Limnology and Oceanography, 34, 1084-1088.
31. Heckmann LH, Connon R, Hutchinson TH, et al,. (2006) Expression of target and reference genes in Daphnia magna exposed to ibuprofen. BMC Genomics, 7, 175-182.
32. Hietala J, Reinikainen M, Walls M, (1995) Variation in life-history responses of daphnia to toxic microcystis-aeruginosa. Journal of Plankton Research, 17, 2307-2318. (Pubitemid 3022489)
33. Ingvarsson PK, (2005) Molecular population genetics of herbivore-induced protease inhibitor genes in European Aspen (Populus tremula L., Salicaceae). Molecular Biology and Evolution, 22, 1802-1812. (Pubitemid 41191507)
34. Jongsma MA, Beekwilder MJ, (2011) Co-evolution of insect proteases and plant protease inhibitors. Current protein and peptide Science, 12, 437-447.
35. Jongsma MA, Bolter C, (1997) The adaptation of insects to plant protease inhibitors. Journal of Insect Physiology, 43, 885-895. (Pubitemid 27521869)
36. Kaltz O, Shykoff JA, (1998) Local adaptation in host-parasite systems. Heredity, 81, 361-370. (Pubitemid 28519475)
37. Lampert W, Rothhaupt KO, (1991) Alternating dynamics of rotifers and Daphnia magna in a shallow lake. Archiv für Hydrobiologie, 120, 447-456.
38. Lampert W, Trubetskova I, (1996) Juvenile growth rate as a measure of fitness in Daphnia. Functional Ecology, 10, 631-635.
39. Lampert W, Fleckner W, Rai H, Taylor BE, (1986) Phytoplankton control by grazing zooplankton-A study on the spring clear-water phase. Limnology and Oceanography, 31, 478-490.
40. Lemaire V, Brusciotti S, van Gremberghe I, Vyverman W, Vanoverbeke J, DeMeester L, (2011) Genotype × genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea Daphnia. Evolutionary Applications, 5, 168-182.
41. Liess A, Hillebrand H, (2004) Invited review: direct and indirect effects in herbivore- periphyton interactions. Archiv für Hydrobiologie, 159, 433-453. (Pubitemid 38522159)
42. Lürling M, (2003) Daphnia growth on microcystin-producing and microcystin-free Microcystis aeruginosa in different mixtures with the green alga Scenedesmus obliquus. Limnology and Oceanography, 48, 2214-2220. (Pubitemid 37538072)
43. Lürling M, 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. Environmental Toxicology & Chemistry, 22, 1281-1287. (Pubitemid 37092482)
44. Martin C, Oberer L, Ino T, et al,. (1993) Cyanopeptolins, new depsipeptides from the cyanobacterium Microcystis sp. PCC 7806. Journal of Antibiotics, 46, 1550-1556. (Pubitemid 23324894)
45. Martin-Creuzburg D, Von Elert E, (2009) Ecological significance of sterols in aquatic foodwebs. In: Lipids in Aquatic Ecosystems (eds, Arts MT, Brett M, Kainz M,), pp. 43-64. Springer, Dordrecht, Heidelberg, London, New York.
46. Mazumdar-Leighton S, Broadway RM, (2001a) Identification of six chymotrypsin cDNAs from larval midguts of Helicoverpa zea and Agrotis ipsilon feeding on the soybean (Kunitz) trypsin inhibitor. Insect Biochemistry and Molecular Biology, 31, 633-644. (Pubitemid 32373910)
47. Mazumdar-Leighton S, Broadway RM, (2001b) Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochemistry and Molecular Biology, 31, 645-657. (Pubitemid 32373911)
48. Mello MO, Silva-Filho MC, (2002) Plant-insect interactions: an evolutionary arms race between two distinct defense mechanisms. Brazilian Journal of Plant Physiology, 14, 71-81. (Pubitemid 36251097)
49. Mosolov VV, Valueva TA, (2005) Proteinase inhibitors and their function in plants: a review. Applied Biochemistry and Microbiology, 41, 227-246. (Pubitemid 40768525)
50. Patankar AG, Giri AP, Harsulkar AM, et al,. (2001) Complexity in specificities and expression of Helicoverpa armigera gut proteinases explains polyphagous nature of the insect pest. Insect Biochemistry and Molecular Biology, 31, 453-464. (Pubitemid 32216757)
51. Pijanowska J, Weider LJ, Lampert W, (1993) Predator-mediated genotypic shifts in a prey population: experimental evidence. Oecologia, 96, 40-42. (Pubitemid 24411501)
52. Repka S, (1997) Effects of food type on the life history of Daphnia clones from lakes differing in trophic state: I. Daphnia galeata feeding on Scenedesmus and Oscillatoria. Freshwater Biology, 38, 675-683. (Pubitemid 28065540)
53. Rohrlack T, Christoffersen K, Friberg-Jensen U, (2005) Frequency of inhibitors of daphnid trypsin in the widely distributed cyanobacterial genus Planktothrix. Environmental Microbiology, 7, 1667-1669. (Pubitemid 41345908)
54. Sarnelle O, (2007) Initial conditions mediate the interaction between Daphnia and bloom- forming cyanobacteria. Limnology and Oceanography, 52, 2120-2127. (Pubitemid 47612135)
55. Sarnelle O, Wilson AE, (2005) Local adaptation of Daphnia pulicaria to toxic cyanobacteria. Limnology and Oceanography, 50, 1565-1570. (Pubitemid 41356437)
56. Schwarzenberger A, Courts C, Von Elert E, (2009) Target gene approaches: gene expression in Daphnia magna exposed to predator-borne kairomones or to microcystin-producing and microcystin-free Microcystis aeruginosa. BMC Genomics, 10, 527.
57. Schwarzenberger A, Zitt A, Kroth P, Mueller S, Von Elert E, (2010) Gene expression and activity of digestive proteases in Daphnia: effects of cyanobacterial protease inhibitors. BMC Physiology, 10. doi: 10.1186/1472-6793-10-6.
58. Schwerin S, Zeis B, Lamkemeyer T, et al,. (2009) Acclimatory responses of the Daphnia pulex proteome to environmental changes. II. Chronic exposure to different temperatures (10 and 20°C) mainly affects protein metabolism. BMC Physiology, 9. doi: 10.1186/1472-6793-9-8
59. Strauss SY, Agrawal AA, (1999) The ecology and evolution of plant tolerance to herbivory. Trends in Ecology and Evolution, 14, 179-185. (Pubitemid 29189980)
60. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599. (Pubitemid 47236692)
61. Threlkeld ST, (1979) Midsummer dynamics of 2 Daphnia species in Wintergreen Lake, Michigan. Ecology, 60, 165-179.
62. Trimbee AM, Prepas EE, (1987) Evaluation of total phosphorus as a predictor of the relative biomass of blue-green-algae with emphasis on Alberta Lakes. Canadian Journal of Fisheries and Aquatic Sciences, 44, 1337-1342.
63. 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. Limnology and Oceanography, 47, 1764-1773. (Pubitemid 36016834)
64. Von Elert E, Jüttner F, (1997) Phosphorus limitation not light controls the exudation of allelopathic compounds by Trichormus doliolum. Limnology and Oceanography, 42, 1796-1802. (Pubitemid 127687996)
65. Von Elert E, Agrawal MK, Gebauer C, et al,. (2004) Protease activity in guts of Daphnia magna: evidence for trypsin and chymotrypsin enzymes. Comparative Biochemistry and Physiology Part B, 137, 287-296. (Pubitemid 38429741)
66. Von Elert E, Oberer L, Merkel P, Huhn T, Blom JF, (2005) Cyanopeptolin 954, a novel chlorine-containing chymotrypsin-inhibitor of Microcystis aeruginosa NIVA Cya43. Journal of Natural Products, 68, 1324-1327. (Pubitemid 41499423)
67. Von Elert E, Zitt A, Schwarzenberger A, (2012) Inducible tolerance in Daphnia magna to dietary protease inhibitors. Journal of Experimental Biology, 215, 2051-2059.
68. Watanabe H, Tatarazako N, Oda S, et al,. (2005) Analysis of expressed sequence tags of the water flea Daphnia magna. Genome, 48, 606-609. (Pubitemid 41483418)
69. Weckesser J, Martin C, Jakobi C, (1996) Cyanopeptolins, depsipeptides from cyanobacteria. Systematic and Applied Microbiology, 19, 133-138. (Pubitemid 26280197)