Daphnia magna tolerance to toxic cyanobacteria in the presence of an opportunistic infection within an evolutionary perspective

Authors

  • Alice Boudry Aquatic Biology, IRF Life Sciences, Science & Technology, KU Leuven, Campus Kortrijk
  • Sarah Devliegere Aquatic Biology, IRF Life Sciences, Science & Technology, KU Leuven, Campus Kortrijk
  • Shira Houwenhuyse Aquatic Biology, IRF Life Sciences, Science & Technology, KU Leuven, Campus Kortrijk
  • Lucas Clarysse Aquatic Biology, IRF Life Sciences, Science & Technology, KU Leuven, Campus Kortrijk
  • Emilie Macke Aquatic Biology, IRF Life Sciences, Science & Technology, KU Leuven, Campus Kortrijk
  • Isabel Vanoverberghe Aquatic Biology, IRF Life Sciences, Science & Technology, KU Leuven, Campus Kortrijk
  • Ellen Decaestecker Aquatic Biology, IRF Life Sciences, Science & Technology, KU Leuven, Campus Kortrijk

DOI:

https://doi.org/10.26496/bjz.2020.75

Keywords:

Daphnia, toxic cyanobacteria, biotic interactions

Abstract

In aquatic environments, interactions between cyanobacteria and their grazers are crucial for ecosystem functioning. Cyanobacteria are photosynthetic prokaryotes, which are able to produce large blooms and associated toxins, some of which are able to suppress grazer fitness. Cyanobacterial blooms are intensified by global warming and eutrophication. In our experiments, the tolerance of Daphnia magna (Straus, 1820), an efficient grazer of toxic cyanobacteria, was studied. We used different D. magna clones sampled from different sediment depths, which corresponded to different time periods of eutrophication. Our results showed that different clones had a different tolerance towards the toxic cyanobacterial species, Microcystis aeruginosa, confirming the presence of genetic variation in D. magna tolerance to cyanobacteria. However, there was not a significant adaptive effect of sediment depth. As expected, in general under controlled, infection-free conditions M. aeruginosa reduced D. magna survival. However, a coincidental, non-intended opportunistic fungal infection in a first experiment allowed us to compare the response of D. magna to M. aeruginosa in infected individuals and non-infected individuals (from a second experiment). In the presence of this opportunistic infection, there was no negative effect of M. aeruginosa in the D. magna clones, suggesting that exposure to the infection provided protection for Daphnia individuals towards Microcystis. Biotic interactions can thus be important in the interpretation of cyanobacterial effects in zooplankton grazers and in finding appropriate solutions to reduce the occurrence of cyanobacterial blooms.

References

Alberdi A., Aizpurua O., Bohmann K., Zepeda-Mendoza M.L. & Gilbert M.T.P. (2016). Do vertebrate gut metagenomes confer rapid ecological adaptation? Trends in Ecology and Evolution 31: 689–699. https://doi.org/10.1016/j.tree.2016.06.008

Brendonck L. & De Meester L. (2003). Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491: 65. https://doi.org/10.1023/A:1024454905119

Coopman M., Muylaert K., Lange B., Reyserhove L. & Decaestecker E. (2014). Context dependency of infectious disease: the cyanobacterium Microcystis aeruginosa decreases White Fat Cell Disease in Daphnia magna. Freshwater Biology 59: 714–723. https://doi.org/10.1111/fwb.12298

Cousyn C., De Meester L., Colbourne J.K., Brendonck L., Verschuren D. & Volckaert F. (2001). Rapid, local adaptation of zooplankton behavior to changes in predation pressure in the absence of neutral genetic changes. Proceeding of the National Academy of Sciences 98: 6256–6260. https://doi.org/10.1073/pnas.111606798

Decaestecker E., Levever C., De Meester L., Ebert E. (2004). Haunted by the past: evidence for dormant stage banks of microparasites and epibionts of Daphnia. Limnology and Oceanography 49: 1355–1364. https://doi.org/10.4319/lo.2004.49.4_part_2.1355

Decaestecker E., Gaba S., Raeymaekers J.A.M., Stoks R., Van Kerckhoven L., Ebert D. & De Meester L. (2007). Host–parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 450: 870–874. https://doi.org/10.1038/nature06291

Decaestecker E., De Gersem H., Michalakis Y. & Raeymaekers J. (2013). Damped long-term host-parasite Red Queen coevolutionary dynamics: a reflection of dilution effects? Ecology Letters 16: 1455–1462. https://doi.org/10.1111/ele.12186

De Figueiredo D.R., Azeiteiro U.M., Esteves S.M., Gonçalves F.J.M. & Pereira M.J. (2004). Microcystin-producing blooms – A serious global public health issue. Ecotoxicology and Environmental Safety 59: 151–163. https://doi.org/10.1016/j.ecoenv.2004.04.006

Frenken T., Wierenga J., van Donk E., Declerck S.A.J., De Senerpont Domis L.N., Rohrlack T. & van de waal D.B. (2018). Fungal parasites of a toxic inedible cyanobacterium provide food to zooplankton. Limnology and Oceanography 63 (6): 2384–2393. https://doi.org/10.1002/lno.10945

Ghadouani A., Pinel-Alloul B. & Prepas E.E. (2003). Effects of experimentally induced cyano-bacterial blooms on crustacean zooplankton communities. Freshwater Biology 48: 363–381. https://doi.org/10.1046/j.1365-2427.2003.01010.x

Guillard R.R. & Lorenzen C.J. (1972). Yellow-green algae with chlorophyllide C1, 2. Journal of Phycology 8: 10–14. https://doi.org/10.1111/j.1529-8817.1972.tb03995.x

Hairston N.G., Lampert W., Caceres C.E., Holtmeier C.L., Weider L.J., Gaedke U., Fischer J.M., Fox J.A. & Post D.M. (1999). Lake ecosystems: Rapid evolution revealed by dormant eggs. Nature 401: 446. https://doi.org/10.1038/46731

Jia Y., Du J., Song F., Zhao G. & Tian X. (2012). A fungus capable of degrading Microcystin-LR in the algal culture of Microcystis aeruginosa PCC7806. Applied Biochemistry and Biotechnology 166: 987–996. https://doi.org/10.1007/s12010-011-9486-6

Kemal A.G., Hansson L.A. & Lürling M. (2014). Understanding cyanobacteria-zooplankton inter-actions in a more eutrophic world. Freshwater Biology 59: 1783–1798. https://doi.org/10.1111/fwb.12393

Kuster C.J. & Von Elert E. (2013). Interspecific differences between D. pulex and D. magna in tolerance to cyanobacteria with protease inhibitors. PloS one 8: 1–8. https://doi.org/10.1371/journal.pone.0062658

Lemaire V., Brusciotti S., Van Gremberghe I., Vyverman W. & Vanoverbeke J. (2012). Genotype × genotype interactions between the toxic cyanobacterium Microcystis and its grazer, the waterflea. Evolutionary Applications 5: 168–182. https://doi.org/10.1111/j.1752-4571.2011.00225.x

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. https://doi.org/10.4319/lo.2003.48.6.2214

Macke E., Callens M., De Meester L. & Decaestecker E. (2017a). Host genotype-dependent gut microbiota drives zooplankton tolerance to toxic cyanobacteria. Nature Communications 8: 1608. https://doi.org/10.1038/s41467-017-01714-x

Macke E., Tasiemski A., Massol F., Callens M. & Decaestecker E. (2017b). Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos 126: 508–538. https://doi.org/10.1111/oik.03900

Macke E., Callens M., Massol F., Vanoverberghe I., De Meester L. & Decaestecker E. (2020). Diet and genotype of an aquatic invertebrate affect the composition of free-living microbial communities. Frontiers in Microbiology in press. https://doi.org/10.3389/fmicb.2020.00380

Mohamed Z.A., Hashem M. & Alamri S.A. (2014). Growth inhibition of the cyanobacterium Microcystis aeruginosa and degradation of its microcystin toxin by the fungus Trichoderma citrinoviride. Toxicon 86: 51–58. https://doi.org/10.1016/j.toxicon.2014.05.008

Moheimani N.R., Borowitzka M.A., Isdepsky A. & Sing S.F. (2013). Standard Methods for Measuring Growth of Algae. In: Borowitzka M.A. & Moheimani N.R. (eds) Algae for Biofuels and Energy: 265–284. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5479-9

Pauwels K., Stok R., Decaestecker E. & De Meester L. (2007) Evolution of Heat Shock protein expression in a natural population of Daphnia magna. American Naturalist 170: 800–805. https://doi.org/10.1086/521956

Peretyatko A., Teissier S., De Backer S. & Triest L. (2012). Biomanipulation of hypereutrophic ponds: when it works and why it fails. Environmental Monitoring and Assessment 184: 1517–1531. https://doi.org/10.1007/s10661-011-2057-z

Reyershove L., Samaey G., Muylaert K., Coppé V., Van Colen W. & Decaestecker E. (2017). A historical perspective of nutrient change impact on an infectious disease in Daphnia. Ecology 98 (11): 2784–2798. https://doi.org/10.1002/ecy.1994

Sánchez K.F., Huntley N., Duffy M.A. & Hunter M.D. (2019). Toxins or medicines? Phytoplankton diets mediate host and parasite fitness in a freshwater system. Proceedings of the Royal Society B 286: 1894. https://doi.org/10.1098/rspb.2018.2231

Stoks R., Govaert L., Pauwels K., Jansen B. & De Meester L. (2016). Resurrecting complexity: the interplay of plasticity and rapid evolution in the multiple trait response to changes in predation pressure in the water flea Daphnia magna. Ecology Letters 19: 180–190. https://doi.org/10.1111/ele.12551

Toenshoff E.R., Fields P.D., Bourgeois Y.X. & Ebert D. (2018). The end of a 60-year riddle: Identification and genomic characterization of an Iridovirus, the causative agent of White Fat Cell Disease in zooplankton. G3: Genes, Genomes, Genetics 8 (4): 1259–1272. https://doi.org/10.1534/g3.117.300429

Visser P.M., Verspagen J.M.H., Sandrini G., Stal L.J., Matthijs H.C.P., Davis T.W., Pearl H.W. & Huisman J. (2016). How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae 54: 145–159. https://doi.org/10.1016/j.hal.2015.12.006

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Published

2020-07-07

How to Cite

Boudry, A., Devliegere, S., Houwenhuyse, S., Clarysse, L., Macke, E., Vanoverberghe, I., & Decaestecker, E. (2020). Daphnia magna tolerance to toxic cyanobacteria in the presence of an opportunistic infection within an evolutionary perspective. Belgian Journal of Zoology, 150. https://doi.org/10.26496/bjz.2020.75

Issue

Vol. 150 (2020)

Section

Articles

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