Proteomic analysis of Daphnia magna hints at molecular pathways involved in defensive plastic responses

BMC Genomics

Christian Laforsch²  Georg J Arnold¹  Thomas Fröhlich¹  Kathrin A Otte² 

[1]Laboratory for Functional Genome Analysis (LAFUGA), Gene Center, Ludwig-Maximilians-University Munich, Feodor-Lynen-Str. 25, 81377 München, Germany

[2]Animal Ecology I, Bayreuth University, 95440 Bayreuth, Germany

关键词: Proteomics;    2D-DIGE;    Predator-prey interaction;    Inducible defence;    Phenotypic plasticity;    Daphnia;   

Others  :  1217429
DOI  :  10.1186/1471-2164-15-306

 received in 2013-12-30, accepted in 2014-04-07,  发布年份 2014

【 摘 要 】

Background

Phenotypic plasticity in defensive traits occurs in many species when facing heterogeneous predator regimes. The waterflea Daphnia is well-known for showing a variety of these so called inducible defences. However, molecular mechanisms underlying this plasticity are poorly understood so far. We performed proteomic analysis on Daphnia magna exposed to chemical cues of the predator Triops cancriformis. D. magna develops an array of morphological changes in the presence of Triops including changes of carapace morphology and cuticle hardening.

Results

Using the 2D-DIGE technique, 1500 protein spots could be matched and quantified. We discovered 179 protein spots with altered intensity when comparing Triops exposed animals to a control group, and 69 spots were identified using nano-LC MS/MS. Kairomone exposure increased the intensity of spots containing muscle proteins, cuticle proteins and chitin-modifying enzymes as well as enzymes of carbohydrate and energy metabolism. The yolk precursor protein vitellogenin decreased in abundance in 41 of 43 spots.

Conclusion

Identified proteins may be either directly involved in carapace stability or reflect changes in energy demand and allocation costs in animals exposed to predator kairomones. Our results present promising candidate proteins involved in the expression of inducible defences in Daphnia and enable further in depth analysis of this phenomenon.

【 授权许可】

   
2014 Otte et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

【 参考文献 】

• [1]Bradshaw AD: Evolutionary significance of phenotypic plasticity in plants. Adv Genet 1965, 13(1):115-155.
• [2]Pigliucci M: Phenotypic Plasticity: Beyond Nature and Nurture. Baltimore: Johns Hopkins University Press; 2001.
• [3]Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH: Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 1995, 10(5):212-217.
• [4]Agrawal AA: Phenotypic plasticity in the interactions and evolution of species. Science 2001, 294(5541):321-326. doi:10.1126/science.1060701
• [5]Tollrian R, Harvell CD: The evolution of inducible defenses: current ideas. Ecol Evol Inducible Defenses 1999, 306-321.
• [6]Riessen HP: Costs of predator-induced morphological defences in Daphnia. Freshwater Biol 2012, 57(7):1422-1433. doi:10.1111/j.1365-2427.2012.02805.x
• [7]Ebert D: Ecology, Epidemiology and Evolution of Parasitism in Daphnia. Bethesda (MD): National Library of Medicine (US), National Center for Biotechnology Information 2005; http://www.ncbi.nlm.nih.gov/books/NBK2036/ webcite
• [8]Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, Bauer DJ, Cáceres CE, Carmel L, Casola C, Choi J-H, Detter JC, Dong Q, Dusheyko S, Eads BD, Fröhlich T, Gerlach D, Hatcher P, Jogdeo S, Krijgsveld J, Kriventseva EV, Kültz D, Laforsch C, Lindquist E, Lopez J, Geiler-Samerotte Ka, et al.: The ecoresponsive genome ofDaphnia pulex. Science 2011, 331(6017):555-561. doi:10.1126/science.1197761
• [9]Laforsch C, Tollrian R: Cyclomorphosis and phenotypic changes. Vol. 3. Encyclopedia Inland Waters 2009, 3:643-650.
• [10]Weider L, Pijanowska J: Plasticity of Daphnia life histories in response to chemical cues from predators. Oikos 1993, 67(3):385-392.
• [11]Riessen H: Predator-induced life history shifts in Daphnia: a synthesis of studies using meta-analysis. Can J Fisheries Aquat Sci 1999, 56:2487-2494.
• [12]De Meester L, Weider L: Depth selection behavior, fish kairomones, and the life histories ofDaphnia hyalina x galeata hybrid clones. Limnology Oceanography 1999, 44(5):1248-1258.
• [13]Dodson S, Havel J: Indirect prey effects: some morphological and life history responses ofDaphnia pulex exposed toNotonecta undulata. Limnology Oceanography 1988, 33(6):1274-1285.
• [14]Lampert W: The adaptive significance of diel vertical migration of zooplankton. Funct Ecol 1989, 3(1):21-27.
• [15]De Meester L: Genotype, fish-mediated chemical, and phototactic behavior inDaphnia magna. Ecology 1993, 74(5):1467-1474.
• [16]Krueger D, Dodson S: Embryological induction and predation ecology inDaphnia pulex. Limnology Oceanography 1981, 26(2):219-223.
• [17]Tollrian R, Laforsch C: Linking predator kairomones and turbulence: synergistic effects and ultimate reasons for phenotypic plasticity inDaphnia cucullata. Archiv für Hydrobiologie 2006, 167(1):135-146. doi:10.1127/0003-9136/2006/0167-0135
• [18]Petrusek A, Tollrian R, Schwenk K, Haas A, Laforsch C: A “crown of thorns” is an inducible defense that protects Daphnia against an ancient predator. Proc Nat Acad Sci USA 2009, 106(7):2248-2252. doi:10.1073/pnas.0808075106
• [19]Dodson S: Predation ofHeterocope septentrionalis on two species of Daphnia: morphological defenses and their cost. Ecology 1984, 65(4):1249-1257.
• [20]Laforsch C, Ngwa W, Grill W, Tollrian R: An acoustic microscopy technique reveals hidden morphological defenses in Daphnia. Proc Nat Acad Sci USA 2004, 101(45):15911-15914. doi:10.1073/pnas.0404860101
• [21]Rabus M, Söllradl T, Clausen-Schaumann H, Laforsch C: Uncovering ultrastructural defences inDaphnia magna – an interdisciplinary approach to assess the predator-induced fortification of the carapace. PloS one 2013., 8(6) doi:10.1371/journal.pone.0067856
• [22]Ebert D: A genome for the environment. 2011, 331(6017):539-540. doi:10.1126/science.1202092
• [23]Tollrian R, Leese F: Ecological genomics: steps towards unraveling the genetic basis of inducible defenses in Daphnia. BMC Biol 2010., 8(51) doi:10.1186/1741-7007-8-51
• [24]Pijanowska J, Kloc M: Daphnia response to predation threat involves heat-shock proteins and the actin and tubulin cytoskeleton. Genesis 2004, 38(2):81-86. doi:10.1002/gene.20000
• [25]Pauwels K, Stoks R, de Meester L: Coping with predator stress: interclonal differences in induction of heat-shock proteins in the water fleaDaphnia magna. J Evol Biol 2005, 18(4):867-872. doi:10.1111/j.1420-9101.2005.00890.x
• [26]Schwarzenberger A, Courts C, von Elert E: Target gene approaches: Gene expression inDaphnia magna exposed to predator-borne kairomones or to microcystin-producing and microcystin-free Microcystis aeruginosa. BMC Genom 2009., 10(527) doi:10.1186/1471-2164-10-527
• [27]Jansen M, Vergauwen L, Vandenbrouck T, Knapen D, Dom N, Spanier KI, Cielen A, De Meester L: Gene expression profiling of three different stressors in the water fleaDaphnia magna. Ecotoxicology 2013, 22(5):900-914. doi:10.1007/s10646-013-1072-y
• [28]Vogel C, Abreu RDS, Ko D, Le S-Y, Burns SC, Sandhu D, Boutz DR, Marcotte EM, Penalva LO, Shapiro Ba: Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol Syst Biol 2010., 6(400) doi:10.1038/msb.2010.59
• [29]Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M: Global quantification of mammalian gene expression control. Nature 2011, 473(7347):337-342. doi:10.1038/nature10098
• [30]Benzie JAH: The Genus Daphnia (including Daphniopsis): (Anomopoda, Daphniidae). vol. 21. Ghent: Kenobi Productions; 2005
• [31]Rabus M, Laforsch C: Growing large and bulky in the presence of the enemyDaphnia magna gradually switches the mode of inducible morphological defences. Funct Ecol 2011, 25(5):1137-1143. doi:10.1111/j.1365-2435.2011.01840.x
• [32]Rabus M, Waterkeyn A, van Pottelbergh N, Brendonck L, Laforsch C: Interclonal variation, effectiveness and long-term implications of Triops-induced morphological defences inDaphnia magna Strauss. J Plankton Res 2012, 34(2):152-160. doi:10.1093/plankt/fbr092
• [33]Fröhlich T, Arnold GJ, Fritsch R, Mayr T, Laforsch C: LC-MS/MS-based proteome profiling inDaphnia pulex andDaphnia longicephala: theDaphnia pulex genome database as a key for high throughput proteomics in Daphnia. BMC Genom 2009., 10(171) doi:10.1186/1471-2164-10-171
• [34]Zeis B, Lamkemeyer T, Paul RJ, Nunes F, Schwerin S, Koch M, Schütz W, Madlung J, Fladerer C, Pirow R: Acclimatory responses of theDaphnia pulex proteome to environmental changes. I. Chronic exposure to hypoxia affects the oxygen transport system and carbohydrate metabolism. BMC Physiol 2009., 9(7) doi:10.1186/1472-6793-9-7
• [35]Schwerin S, Zeis B, Lamkemeyer T, Paul RJ, Koch M, Madlung J, Fladerer C, Pirow R: Acclimatory responses of theDaphnia pulex proteome to environmental changes. II. Chronic exposure to different temperatures (10°C and 20°C) mainly affects protein metabolism. BMC Physiol 2009., 9(8) doi:10.1186/1472-6793-9-8
• [36]Kemp CJ, Kültz D: Controlling Proteome Degradation inDaphnia pulex. J Exp Zool 2012, 317(10):645-651. doi:10.1002/jez.1766
• [37]Schwarzenberger A, Zitt A, Kroth P, Mueller S, Von Elert E: Gene expression and activity of digestive proteases in Daphnia: effects of cyanobacterial protease inhibitors. BMC Physiol 2010., 10(6)
• [38]Laforsch C, Tollrian R: Embryological aspects of inducible morphological defenses in Daphnia. J Morphol 2004, 262(3):701-707.
• [39]Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman W-H, Pagès F, Trajanoski Z, Galon J: ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 2009, 25(8):1091-1093. doi:10.1093/bioinformatics/btp101
• [40]Lima SL, Dill LM: Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 1990, 68(4):619-640.
• [41]Herzog Q, Laforsch C: Modality matters for the expression of inducible defenses: introducing a concept of predator modality. BMC Biol 2013, 11:113. doi:10.1186/1741-7007-11-113 BioMed Central Full Text
• [42]Hettyey A, Vincze K, Zsarnóczai S, Hoi H, Laurila a: Costs and benefits of defences induced by predators differing in dangerousness. J Evol Biol 2011, 24(5):1007-1019. doi:10.1111/j.1420-9101.2011.02233.x
• [43]Dodson S: Zooplankton competition and predation: an experimental test of the size-efficency hypothesis. Ecology 1974, 55(3):605-613.
• [44]Ferl RJ, Manak MS, Reyes MF: The 14-3-3s. Genome Biol 2002, 3(7):1-7.
• [45]Tabunoki H, Shimada T, Banno Y, Sato R, Kajiwara H, Mita K, Satoh J-i: Identification ofBombyx mori 14-3-3 orthologs and the interactor Hsp60. Neurosci Res 2008, 61(3):271-280. doi:10.1016/j.neures.2008.03.007
• [46]Lee S, Feldman R, O’Farrell P: An RNA interference screen identifies a novel regulator of target of rapamycin that mediates hypoxia suppression of translation in Drosophila S2 cells. Mol Biol Cell 2008, 19(October):4051-4061. doi:10.1091/mbc.E08
• [47]Kregel KC: Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol (Bethesda, Md.: 1985) 2002, 92(5):2177-2186. doi:10.1152/japplphysiol.01267.2001
• [48]Sörensen JG, Kristensen TN, Loeschcke V: The evolutionary and ecological role of heat shock proteins. Ecol Lett 2003, 6(11):1025-1037. doi:10.1046/j.1461-0248.2003.00528.x
• [49]Haap T, Köhler H-R: Cadmium tolerance in sevenDaphnia magna clones is associated with reduced hsp70 baseline levels and induction. Aquat Toxicol 2009, 94(2):131-137. doi:10.1016/j.aquatox.2009.06.006
• [50]Nuell M, Stewart D: Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells. Mol Cell Biol 1991, 11(3):1372-1381. doi:10.1128/MCB.11.3.1372.Updated
• [51]Eveleth D, Marsh J: Sequence and expression of the Cc gene, a member of the dopa decarboxylase gene cluster of Drosophila: possible translational regulation. Nucleic Acids Res 1986, 14(15):6169-6184.
• [52]Arbouzova NI, Zeidler MP: JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Dev (Cambridge, England) 2006, 133(14):2605-2616. doi:10.1242/dev.02411
• [53]Mukherjee T, Hombría JC-G, Zeidler MP: Opposing roles for Drosophila JAK/STAT signalling during cellular proliferation. Oncogene 2005, 24(15):2503-2511. doi:10.1038/sj.onc.1208487
• [54]Subramoniam T: Mechanisms and control of vitellogenesis in crustaceans. Fisheries Sci 2010, 77(1):1-21. doi:10.1007/s12562-010-0301-z
• [55]Sappington TW, Raikhel AS: Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem Mol Biol 1998, 28(5-6):277-300.
• [56]Romano M, Rosanova P, Anteo C, Limatola E: Vertebrate yolk proteins: a review. Mol Reprod Dev 2004, 69(1):109-116. doi:10.1002/mrd.20146
• [57]Raikhel AS, Dhadialla TS: Accumulation of yolk proteins in insect oocytes. Ann Rev Entomol 1992, 37:217-251. doi:10.1146/annurev.en.37.010192.001245
• [58]Byrne B, Gruber M, Ab G: The evolution of egg yolk proteins. Prog Biophys Mol Biol 1989, 53:33-69.
• [59]Stibor H: The role of yolk protein dynamics and predator kairomones for the life history ofDaphnia magna. Ecology 2002, 83(2):362-369. doi:10.2307/2680020
• [60]Boersma M, Spaak P, Meester LD: Predator-mediated plasticity in morphology, life history, and behavior of Daphnia: the uncoupling of responses. Am Nat 1998, 152(2):237-248.
• [61]Pauwels K, Stoks R, De Meester L: Enhanced anti-predator defence in the presence of food stress in the water fleaDaphnia magna. Func Ecol 2010, 24(2):322-329. doi:10.1111/j.1365-2435.2009.01641.x
• [62]Coors A, Hammers-Wirtz M, Ratte HT: Adaptation to environmental stress inDaphnia magna simultaneously exposed to a xenobiotic. Chemosphere 2004, 56(4):395-404. doi:10.1016/j.chemosphere.2004.04.025
• [63]Hesse O, Engelbrecht W, Laforsch C, Wolinska J: Fighting parasites and predators: how to deal with multiple threats? BMC Ecol 2012., 12(12) doi:10.1186/1472-6785-12-12
• [64]Sheterline P, Clayton J, Sparrow JC: Actin. Oxford: OUP Oxford; 1999.
• [65]Fyrberg EA, Mahaffey JW, Bond BJ, Davidson N: Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell 1983, 33(1):115-123.
• [66]Röper K, Mao Y, Brown NH: Contribution of sequence variation in Drosophila actins to their incorporation into actin-based structures in vivo. J Cell Sci 2005, 118(Pt 17):3937-3948. doi:10.1242/jcs.02517
• [67]Hooper SL, Hobbs KH, Thuma JB: Invertebrate muscles: thin and thick filament structure; molecular basis of contraction and its regulation, catch and asynchronous muscle. Prog Neurobiol 2008, 86(2):72-127. doi:10.1016/j.pneurobio.2008.06.004
• [68]Margulis B, Bobrova I: Major myofibrillar protein content and the structure of mollusc adductor contractile apparatus. Comp Biochem Physiol 1979, 64A:291-298.
• [69]Reimer O, Harms-Ringdahl S: Predator-inducible changes in blue mussels from the predator-free Baltic Sea. Mar Biol 2001, 139(5):959-965. doi:10.1007/s002270100606
• [70]Anderson BG: Regeneration in the carapace ofDaphnia magna. Biol Bull 1933, 64(1):70-85.
• [71]Halcrow K, John S, Brunswick N: The fine structure of the carapace integument ofDaphnia magna. Cell Tissue Res 1976, 276:267-276.
• [72]Andersen SO: Mini-review insect cuticular proteins. Insect Biochem Mol Biol 1995, 25(2):153-176.
• [73]Skinner D, Kumari S: Proteins of the crustacean exoskeleton. Am Zool 1992, 32(3):470-484.
• [74]Vincent JFV, Wegst UGK: Design and mechanical properties of insect cuticle. Arthropod Struct Dev 2004, 33(3):187-199. doi:10.1016/j.asd.2004.05.006
• [75]de Castro E, Cerutti L, Cuche BA, Hulo N, Bridge A, Bougueleret L, Xenarios I, Sigrist CJa: New and continuing developments at PROSITE. Nucleic Acids Res 2013, 41(Database issue):344-347. doi:10.1093/nar/gks1067
• [76]Reberst JE, Riddifordt LM: Structure and Expression of aManduca sexta larval cuticle gene homologous to drosophila cuticle genes. J Mol Biol 1988, 203:411-423.
• [77]Andersen SO: Amino acid sequence studies on endocuticular proteins from the desert locust,Schistocerca gregaria. Insect Biochem Mol Biol 1998, 28(5-6):421-434.
• [78]Arakane Y, Dixit R, Begum K, Park Y, Specht CA, Merzendorfer H, Kramer KJ, Muthukrishnan S, Beeman RW: Analysis of functions of the chitin deacetylase gene family inTribolium castaneum. Insect Biochem Mol Biol 2009, 39(5-6):355-365. doi:10.1016/j.ibmb.2009.02.002
• [79]Laforsch C, Beccara L, Tollrian R: Inducible defenses: The relevance of chemical alarm cues in Daphnia. Limnol Oceanography 2006, 51(3):1466-1472. doi:10.4319/lo.2006.51.3.1466
• [80]Huang Y, Niu B, Gao Y, Fu L, Li W: CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 2010, 26(5):680-682. doi:10.1093/bioinformatics/btq003
• [81]R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2011. http://www.r-project.org/ webcite
• [82]Geer LY, Marchler-Bauer A, Geer RC, Han L, He J, He S, Liu C, Shi W, Bryant SH: The NCBI BioSystems database. Nucleic Acids Res 2010, 38(suppl 1):492-496.
• [83]Grant BJ, Rodrigues APC, ElSawy KM, McCammon JA, Caves LSD: Bio3D: An R package for the comparative analysis of protein structures. Bioinformatics 2006, 22:2695-2696.
• [84]Durinck S, Spellman PT, Birney E, Huber W: Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nature Protocols 2009, 4(8):1184-91.
• [85]Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T: Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27(3):431-432. doi:10.1093/bioinformatics/btq675
• [86]Bindea G, Galon J, Mlecnik B: CluePedia Cytoscape plugin: pathway insights using integrated experimental and in silico data. Bioinformatics (Oxford, England) 2013, 29(5):661-663. doi:10.1093/bioinformatics/btt019