Proteomic analysis in the model organism Daphnia has the potential to unravel molecular pathways involved in phenotypic changes in response to changing environmental conditions
Abstract
The crustacean genus Daphnia holds a key position in aquatic ecosystems rendering it an important model organism in environmental research. Its enormous sensitivity to environmental changes is often accompanied by complex plastic responses resulting in different phenotypes from the same genetic background. This plasticity enables Daphnia to survive in heterogeneous environments. The molecular underpinning of these responses are of general interest as they may not only reveal mechanisms of plastic adaptation but also help to predict the impact of global environmental changes. Proteomics is especially suitable to analyse such molecular mechanisms, as proteins are the functional key players of most biochemical processes. In this review, we highlight crucial methodological steps for performing high-quality Daphnia proteomics. Furthermore, we report proteome studies which are able to link genotype and phenotype for a variety of plastic traits, emphasizing the great potential of Daphnia as a model organism for studying the effects of fluctuating and changing environments.
Keywords
Daphnia Proteomics Molecular mechanisms Phenotypic plasticityNotes
Acknowledgements
Funding was provided by European Science Foundation (Grant No. STRESSFLEA).
References
- Aebersold, R. & M. Mann, 2003. Mass spectrometry-based proteomics. Nature 422: 198–207.CrossRefPubMedPubMedCentralGoogle Scholar
- Agrawal, M. K., A. Zitt, D. Bagchi, J. Weckesser, S. N. Bagchi & E. von Elert, 2005. Characterization of proteases in guts of Daphnia magna and their inhibition by Microcystis aeruginosa PCC 7806. Environmental Toxicology 20: 314–322.CrossRefPubMedPubMedCentralGoogle Scholar
- Anderson, N. L., J. P. Hofmann, A. Gemmell & J. Taylor, 1984. Global approaches to quantitative analysis of gene-expression patterns observed by use of two-dimensional gel electrophoresis. Clinical Chemistry 30: 2031–2036.PubMedPubMedCentralGoogle Scholar
- Bantscheff, M., S. Lemeer, M. M. Savitski & B. Kuster, 2012. Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Analytical and bioanalytical chemistry 404: 939–965.CrossRefPubMedPubMedCentralGoogle Scholar
- Bantscheff, M., M. Schirle, G. Sweetman, J. Rick & B. Kuster, 2007. Quantitative mass spectrometry in proteomics: a critical review. Analytical and Bioanalytical Chemistry 389: 1017–1031.CrossRefPubMedPubMedCentralGoogle Scholar
- Borgatta, M., C. Hernandez, L. A. Decosterd, N. Chevre & P. Waridel, 2015. Shotgun ecotoxicoproteomics of Daphnia pulex: biochemical effects of the anticancer drug tamoxifen. Journal of Proteome Research 14: 279–291.CrossRefPubMedPubMedCentralGoogle Scholar
- Brzezinski, T. & E. von Elert, 2015. Predator evasion in zooplankton is suppressed by polyunsaturated fatty acid limitation. Oecologia Springer 179: 687–697.CrossRefGoogle Scholar
- Cañas, B., C. Piñeiro, E. Calvo, D. López-Ferrer & J. M. Gallardo, 2007. Trends in sample preparation for classical and second generation proteomics. Journal of Chromatography A 1153: 235–258.CrossRefPubMedPubMedCentralGoogle Scholar
- Colbourne, J. K., M. E. Pfrender, D. Gilbert, W. K. Thomas, A. Tucker, T. H. Oakley, S. Tokishita, A. Aerts, G. J. Arnold, M. K. Basu, D. J. Bauer, C. E. Cáceres, L. Carmel, C. Casola, J.-H. Choi, J. C. Detter, Q. Dong, S. Dusheyko, B. D. Eads, T. Fröhlich, K. A. Geiler-Samerotte, D. Gerlach, P. Hatcher, S. Jogdeo, J. Krijgsveld, E. V. Kriventseva, D. Kültz, C. Laforsch, E. Lindquist, J. Lopez, J. R. Manak, J. Muller, J. Pangilinan, R. P. Patwardhan, S. Pitluck, E. J. Pritham, A. Rechtsteiner, M. Rho, I. B. Rogozin, O. Sakarya, A. Salamov, S. Schaack, H. Shapiro, Y. Shiga, C. Skalitzky, Z. Smith, A. Souvorov, W. Sung, Z. Tang, D. Tsuchiya, H. Tu, H. Vos, M. Wang, Y. I. Wolf, H. Yamagata, T. Yamada, Y. Ye, J. R. Shaw, J. Andrews, T. J. Crease, H. Tang, S. M. Lucas, H. M. Robertson, P. Bork, E. V. Koonin, E. M. Zdobnov, I. V. Grigoriev, M. Lynch & J. L. Boore, 2011. The ecoresponsive genome of Daphnia pulex. Science 331: 555–561.CrossRefPubMedPubMedCentralGoogle Scholar
- Cox, J., M. M. Y. Hein, C. C. A. Luber, I. Paron, N. Nagaraj & M. Mann, 2014. MaxLFQ allows accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction. Molecular & Cellular Proteomics 13: 2513–2526.CrossRefGoogle Scholar
- De Sousa Abreu, R., L. O. Penalva, E. M. Marcotte & C. Vogel, 2009. Global signatures of protein and mRNA expression levels. Molecular BioSystems 5: 1512–1526.PubMedGoogle Scholar
- DeMott, W. R. & D. Shree, 1995. Inhibition of in vitro protein phosphatase activity in three zooplankton species by microcystin-LR, a toxin from cyanobacteria. Archiv für Hydrobiologie Schweizerbart 134: 417–424.Google Scholar
- Denslow, N. D., J. K. Colbourne, D. Dix, J. H. Freedman, C. C. Helbing, S. Kennedy & P. L. Williams, 2007. Selection of Surrogate Animal Species for Comparative Toxicogenomics. Genomic Approaches for Cross-Species Extrapolation in Toxicology. CRC Press, Portland.Google Scholar
- Dircksen, H., S. Neupert, R. Predel, P. Verleyen, J. Huybrechts, J. Strauss, F. Hauser, E. Stafflinger, M. Schneider, K. Pauwels, L. Schoofs & C. J. P. Grimmelikhuijzen, 2011. Genomics, transcriptomics, and peptidomics of Daphnia pulex neuropeptides and protein hormones. Journal of Proteome Research 10: 4478–4504.CrossRefPubMedPubMedCentralGoogle Scholar
- Ebert, D., 2005. Ecology Epidemiology and Evolution of Parasitism in Daphnia. Bethesda, National Library of Medicine (US), National Center for Biotechnology Information.Google Scholar
- Effertz, C., S. Müller & E. Von Elert, 2015. Differential peptide labeling (iTRAQ) in LC-MS/MS based proteomics in Daphnia reveal mechanisms of an antipredator response. Journal of Proteome Research 14: 888–896.CrossRefPubMedPubMedCentralGoogle Scholar
- Effertz, C. & E. von Elert, 2014. Light intensity controls anti-predator defences in Daphnia: the suppression of life-history changes. Proceedings of the Royal Society: Biological Sciences 281: 20133250.CrossRefGoogle Scholar
- Effertz, C. & E. von Elert, 2017. Coupling of anti-predator defences in Daphnia: the importance of light. Hydrobiologia 798: 5–13.CrossRefGoogle Scholar
- Eriksson, J. E., D. Toivola, J. A. O. Meriluoto, H. Karaki, Y. G. Han & D. Hartshorne, 1990. Hepatocyte deformation induced by cyanobacterial toxins reflects inhibition of protein phosphatases. Biochemical and Biophysical Research Communications 173: 1347–1353.CrossRefPubMedPubMedCentralGoogle Scholar
- Feder, M. E. & J.-C. Walser, 2005. The biological limitations of transcriptomics in elucidating stress and stress responses. Journal of Evolutionary Biology 18: 901–910.CrossRefGoogle Scholar
- Fröhlich, T., G. J. Arnold, R. Fritsch, T. Mayr & C. Laforsch, 2009. LC-MS/MS-based proteome profiling in Daphnia pulex and Daphnia longicephala: the Daphnia pulex genome database as a key for high throughput proteomics in Daphnia. BMC Genomics 10: 171.CrossRefPubMedPubMedCentralGoogle Scholar
- Gouw, J. W., J. Krijgsveld & A. J. R. Heck, 2010. Quantitative proteomics by metabolic labeling of model organisms. Molecular & Cellular Proteomics 9: 11–24.CrossRefGoogle Scholar
- Grün, D., M. Kirchner, N. Thierfelder, M. Stoeckius, M. Selbach & N. Rajewsky, 2014. Conservation of mRNA and Protein Expression during Development of C. elegans. Cell Reports 6: 565–577.CrossRefGoogle Scholar
- Gustafsson, S., K. Rengefors & L.-A. Hansson, 2005. Increased consumer fitness following transfer of toxin tolerance to offspring via maternal effects. Ecology 86: 2561–2567.CrossRefGoogle Scholar
- Gygi, S. P., G. L. Corthals, Y. Zhang, Y. Rochon & R. Aebersold, 2000. Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology. Proceedings of the National Academy of Sciences of the United States of America 97: 9390–9395.CrossRefPubMedPubMedCentralGoogle Scholar
- Harris, K. D. M., N. J. Bartlett & V. K. Lloyd, 2012. Daphnia as an emerging epigenetic model organism. Genetics Research International 2012: 1–8.CrossRefGoogle Scholar
- Honkanen, R. E., J. Zwiller, R. E. Moore, S. L. Daily, B. S. Khatra, M. Dukelow & A. L. Boynton, 1990. Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. Journal of Biological Chemistry ASBMB 265: 19401–19404.Google Scholar
- Kemp, C. J. & D. Kültz, 2012. Controlling proteome degradation in Daphnia pulex. Journal of Experimental Zoology 317: 645–651.PubMedGoogle Scholar
- Kim, H., P. Koedrith & Y. Seo, 2015. Ecotoxicogenomic Approaches for understanding molecular mechanisms of environmental chemical toxicity using aquatic invertebrate, Daphnia Model organism. International Journal of Molecular Sciences 16: 12261–12287.CrossRefPubMedPubMedCentralGoogle Scholar
- Klose, J., 1975. Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues. A novel approach to testing for induced point mutations in mammals. Humangenetik 26: 231–243.PubMedGoogle Scholar
- Krijgsveld, J., R. Ketting & T. Mahmoudi, 2003. Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nature Biotechnology 21: 927–931.CrossRefGoogle Scholar
- Kwon, O. K., J. Sim, S. J. Kim, H. R. Oh, D. H. Nam & S. Lee, 2016. Global proteomic analysis of protein acetylation affecting metabolic regulation in Daphnia pulex. Biochimie 121: 219–227.CrossRefGoogle Scholar
- Kwon, O. K., J. Sim, K. N. Yun, J. Y. Kim & S. Lee, 2014. Global phosphoproteomic analysis of Daphnia pulex reveals evolutionary conservation of Ser/Thr/Tyr phosphorylation. Journal of Proteome Research 13: 1327–1335.CrossRefGoogle Scholar
- Lampert, W., 1993. Ultimate causes of diel vertical migration of zooplankton: new evidence for the predator-avoidance hypothesis. In Diel Vertical Migration of Zooplankton: 79–88.Google Scholar
- Lampert, W., 2006. Daphnia: model herbivore, predator and prey. Polish Journal of Ecology 54: 607–620.Google Scholar
- Lampert, W. & J. Grey, 2003. Exploitation of a deep-water algal maximum by Daphnia: a stable-isotope tracer study. Hydrobiologia 500: 95–101.CrossRefGoogle Scholar
- Le, T. H., E. S. Lim, N. H. Hong, S. K. Lee, Y. S. Shim, J. R. Hwang, Y. H. Kim & J. Min, 2013. Proteomic analysis in Daphnia magna exposed to As(III), As(V) and Cd heavy metals and their binary mixtures for screening potential biomarkers. Chemosphere 93: 2341–2348.CrossRefGoogle Scholar
- Lemos, M. F. L., A. M. V. M. Soares, A. C. Correia & A. C. Esteves, 2010. Proteins in ecotoxicology – how, why and why not? Proteomics 10: 873–887.CrossRefPubMedPubMedCentralGoogle Scholar
- Li, H., J. Han, J. Pan, T. Liu, C. E. Parker & C. H. Borchers, 2017. Current trends in quantitative proteomics – an update. Journal of Mass Spectrometry 52: 319–341.CrossRefGoogle Scholar
- Lürling, M., 2003. Effects of microcystin-free and microcystin-containing strains of the cyanobacterium Microcystis aeruginosa on growth of the grazer Daphnia magna. Environmental Toxicology 18: 202–210.CrossRefPubMedPubMedCentralGoogle Scholar
- Lyu, K., Q. Meng, X. Zhu, D. Dai, L. Zhang, Y. Huang & Z. Yang, 2016. Changes in iTRAQ-based proteomic profiling of the cladoceran Daphnia magna exposed to microcystin-producing and microcystin-free Microcystis aeruginosa. Environmental Science & Technology 50: 4798–4807.CrossRefGoogle Scholar
- Miner, B. E., L. De Meester, M. E. Pfrender, W. Lampert & N. G. Hairston, 2012. Linking genes to communities and ecosystems: Daphnia as an ecogenomic model. Proceedings of the Royal Society: Biological Sciences 279: 1873–1882.CrossRefGoogle Scholar
- Morris, M., & S. M. Rogers, 2014. Integrating phenotypic plasticity within an ecological genomics framework: recent insights from the genomics, evolution, ecology, and fitness of plasticity. In Ecological Genomics. Springer, New York: 73–105.Google Scholar
- Nagaraj, N., N. Alexander Kulak, J. Cox, N. Neuhauser, K. Mayr, O. Hoerning, O. Vorm & M. Mann, 2012. System-wide perturbation analysis with nearly complete coverage of the yeast proteome by single-shot ultra HPLC runs on a bench top orbitrap. Molecular & Cellular Proteomics 11: M111.013722.CrossRefGoogle Scholar
- Nagaraj, N., J. R. Wisniewski, T. Geiger, J. Cox, M. Kircher, J. Kelso, S. Pääbo & M. Mann, 2011. Deep proteome and transcriptome mapping of a human cancer cell line. Molecular Systems Biology 7: 1–8.CrossRefGoogle Scholar
- O’Farrell, P. H., 1975. High resolution two-dimensional electrophoresis of proteins. The Journal of Biological Chemistry 250: 4007–4021.PubMedPubMedCentralGoogle Scholar
- Ong, S.-E., B. Blagoev, I. Kratchmarova, D. B. Kristensen, H. Steen, A. Pandey & M. Mann, 2002. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Molecular & Cellular Proteomics 1: 376–386.CrossRefGoogle Scholar
- Otte, K. A., T. Fröhlich, G. J. Arnold & C. Laforsch, 2014. Proteomic analysis of Daphnia magna hints at molecular pathways involved in defensive plastic responses. BMC Genomics 15: 306.CrossRefPubMedPubMedCentralGoogle Scholar
- Otte, K. A., I. Schrank, T. Fröhlich, G. J. Arnold & C. Laforsch, 2015. Interclonal proteomic responses to predator exposure in Daphnia magna may depend on predator composition of habitats. Molecular Ecology 24: 3901–3917.CrossRefPubMedPubMedCentralGoogle Scholar
- Patterson, S. D. & R. H. Aebersold, 2003. Proteomics: the first decade and beyond. Nature Genetics 33(Suppl): 311–323.CrossRefGoogle Scholar
- Petrusek, A., R. Tollrian, K. Schwenk, A. Haas & C. Laforsch, 2009. A “crown of thorns” is an inducible defense that protects Daphnia against an ancient predator. Proceedings of the National Academy of Sciences of the United States of America 106: 2248–2252.CrossRefPubMedPubMedCentralGoogle Scholar
- Puddick, J., M. R. Prinsep, S. A. Wood, S. A. F. Kaufononga, S. C. Cary & D. P. Hamilton, 2014. High levels of structural diversity observed in microcystins from Microcystis CAWBG11 and characterization of six new microcystin congeners. Marine Drugs 12: 5372–5395.CrossRefPubMedPubMedCentralGoogle Scholar
- Rabus, M. & C. Laforsch, 2011. Growing large and bulky in the presence of the enemy: Daphnia magna gradually switches the mode of inducible morphological defences. Functional Ecology 25: 1137–1143.CrossRefGoogle Scholar
- Rabus, M., T. Söllradl, H. Clausen-Schaumann & C. Laforsch, 2013. Uncovering ultrastructural defences in Daphnia magna – an interdisciplinary approach to assess the predator-induced fortification of the carapace. PLoS ONE 8: e67856.CrossRefPubMedPubMedCentralGoogle Scholar
- Ross, P. L., Y. N. Huang, J. N. Marchese, B. Williamson, K. Parker, S. Hattan, N. Khainovski, S. Pillai, S. Dey, S. Daniels, S. Purkayastha, P. Juhasz, S. Martin, M. Bartlet-Jones, F. He, A. Jacobson & D. J. Pappin, 2004. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Molecular & Cellular Proteomics: MCP, 3(12): 1154–1169. https://doi.org/10.1074/mcp.M400129-MCP200.CrossRefGoogle Scholar
- Sadler, T., C. Kuster & E. von Elert, 2014. Seasonal dynamics of chemotypes in a freshwater phytoplankton community – a metabolomic approach. Harmful Algae 39: 102–111.CrossRefGoogle Scholar
- Scheele, G. A., 1975. Two-dimensional gel analysis of soluble proteins. Charaterization of guinea pig exocrine pancreatic proteins. The Journal of Biological Chemistry 250: 5375–5385.PubMedGoogle Scholar
- Schwanhäusser, B., D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen & M. Selbach, 2011. Global quantification of mammalian gene expression control. Nature 473: 337–342.CrossRefPubMedPubMedCentralGoogle Scholar
- Schwarzenberger, A., T. Sadler, S. Motameny, K. Ben-Khalifa, P. Frommolt, J. Altmüller, K. Konrad & E. von Elert, 2014. Deciphering the genetic basis of microcystin tolerance. BMC Genomics 15: 776.CrossRefPubMedPubMedCentralGoogle Scholar
- Schwarzenberger, A., A. Zitt, P. Kroth, S. Mueller & E. Von Elert, 2010. Gene expression and activity of digestive proteases in Daphnia: effects of cyanobacterial protease inhibitors. BMC Physiology 10: 6.CrossRefPubMedPubMedCentralGoogle Scholar
- Schwerin, S., B. Zeis, T. Lamkemeyer, R. J. Paul, M. Koch, J. Madlung, C. Fladerer & R. Pirow, 2009. Acclimatory responses of the Daphnia pulex proteome to environmental changes. II. Chronic exposure to different temperatures (10 °C and 20 °C) mainly affects protein metabolism. BMC Physiology 9: 8.CrossRefPubMedPubMedCentralGoogle Scholar
- Ślusarczyk, M., 1999. Predator-induced diapause in Daphnia magna may require two chemical cues. Oecologia 119: 159–165.CrossRefGoogle Scholar
- Sommer, U., F. Sommer, B. Santer, E. Zöllner, K. Jürgens, C. Jamieson, M. Boersma & K. Gocke, 2003. Daphnia versus copepod impact on summer phytoplankton: functional compensation at both trophic levels. Oecologia 135: 639–647.CrossRefGoogle Scholar
- Stollewerk, A., 2010. The water flea Daphnia-a ‘new’ model system for ecology and evolution? Journal of Biology 9: 2–5.CrossRefGoogle Scholar
- Thompson, A., J. Schäfer., K. Kuhn., S. Kienle., J. Schwarz, G. Schmidt, T. Neumann & C. Hamon, 2003. Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Analytical Chemistry 75(8): 1895–1904.CrossRefGoogle Scholar
- Toumi, H., M. Boumaiza, F. Immel, B. Sohm, V. Felten & J. F. Férard, 2014. Effect of deltamethrin (pyrethroid insecticide) on two clones of Daphnia magna (Crustacea, Cladocera): a proteomic investigation. Aquatic Toxicology 148: 40–47.CrossRefGoogle Scholar
- Toyota, K., S. Miyagawa, Y. Ogino & T. Iguchi, 2016. Microinjection-based RNA interference method in the water flea, Daphnia pulex and Daphnia magna. InTech, Rijeka.CrossRefGoogle Scholar
- Trotter, B., K. A. Otte., K. Schoppmann., R. Hemmersbach., T. Fröhlich., G. J. Arnold & C. Laforsch, 2015. The influence of simulated microgravity on the proteome of Daphnia magna. NPJ Microgravity. https://doi.org/10.1038/npjmgrav.2015.16.CrossRefPubMedPubMedCentralGoogle Scholar
- Unlü, M., M. E. Morgan & J. S. Minden, 1997. Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18: 2071–2077.CrossRefGoogle Scholar
- Via, S., R. Gomulkiewicz, G. De Jong, S. M. Scheiner, C. D. Schlichting & P. H. Van Tienderen, 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends in Ecology & Evolution 10: 212–217.CrossRefGoogle Scholar
- Vincens, P., P. Tarroux & T. Rabilloud, 1987. HERMes: a second generation approach to the automatic analysis of two-dimensional electrophoresis gels. Part V: Data analysis. Electrophoresis 8: 187–199.CrossRefGoogle Scholar
- Von Elert, E., 2012. Information conveyed by chemical cues. Chemical Ecology in Aquatic Systems. https://doi.org/10.1093/acprof:osobl/9780199583096.003.0003.CrossRefGoogle Scholar
- Von Elert, E., M. K. Agrawal, C. Gebauer, H. Jaensch, U. Bauer & A. Zitt, 2004. Protease activity in gut of Daphnia magna: evidence for trypsin and chymotrypsin enzymes. Comparative Biochemistry and Physiology B 137: 287–296.CrossRefGoogle Scholar
- Wasinger, V., S. Cordwell, A. Cerpa-Poljak, J. Yan, A. Gooley, M. Wilkins, M. Duncan, R. Harris, K. Williams & I. Humphrey-Smith, 1995. Progress with gene-product mapping of the Mollicutes: Mycoplasma genitalium. Electrophoresis 7: 453–457.Google Scholar
- Wiese, S., K. A. Reidegeld., H. E. Meyer & B. Warscheid, 2007. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics 7(3): 340–350.CrossRefGoogle Scholar
- Wilkins, M. R., C. Pasquali, R. D. Appel, K. Ou, O. Golaz, J. C. Sanchez, J. X. Yan, A. A. Gooley, G. Hughes, I. Humphery-Smith, K. L. Williams & D. F. Hochstrasser, 1996. From proteins to proteomes: large scale protein identification by two-dimensional electrophoresis and amino acid analysis. Biotechnology 14: 61–65.PubMedPubMedCentralGoogle Scholar
- Zeis, B., T. Lamkemeyer, R. J. Paul, F. Nunes, S. Schwerin, M. Koch, W. Schütz, J. Madlung, C. Fladerer & R. Pirow, 2009. Acclimatory responses of the Daphnia pulex proteome to environmental changes. I. Chronic exposure to hypoxia affects the oxygen transport system and carbohydrate metabolism. BMC Physiology 9: 7.CrossRefPubMedPubMedCentralGoogle Scholar