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Colony formation by the green alga Chlorella vulgaris in response to the competitor Ceratophyllum demersum

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Abstract

In shallow freshwater ecosystems, submerged macrophytes and algae usually compete for nutrients, light and space. Previous studies mainly focused on the growth effects (biomass, growth rate, photosynthetic activities) of algae by submerged macrophytes. The present study found that submerged macrophytes could also have morphological influences on green algae. We used the green alga Chlorella vulgaris and the photosynthetic competitor Ceratophyllum demersum in our experiments. Results revealed the following: (1) both direct contact and extracts of macrophytes could promote colony formation by C. vulgaris; (2) high biomass of macrophytes caused the formation of more and larger colonies; (3) evidence was found to support the hypothesis that competitive pressure promotes facultative rather than constitutive colony formation. This temporary defensive strategy might be the result of increased carbohydrate production and secretion induced by macrophyte competition. After removal of macrophytes, colony cells reverted to individual cells and the accumulated carbohydrates in the colony cells could provide sufficient energy for rapid development of the algae. Thus, the response of C. vulgaris morphology to macrophytes might represent an effective co-evolutionary or co-existence strategy.

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References

  • Agrawal, A. A., 1998. Induced responses to herbivory and increased plant performance. Science 279: 1201–1202.

    Article  CAS  PubMed  Google Scholar 

  • Amsler, C. D., 2001. Induced defences in macroalgae: the herbivore makes a difference. Journal of Phycology 37: 353–356.

    Article  Google Scholar 

  • Anthoni, U., C. Christophersen, J. Øgård Madsen, S. Wium-Andersen & N. Jacobsen, 1980. Biologically active sulphur compounds from the green algal Chara globularis. Phytochemistry 19: 1228–1229.

    Article  CAS  Google Scholar 

  • Bauer, N., U. Blaschke, E. Beutler, E. M. Gross, K. Jenett-Siems, K. Siems & S. Hilt, 2009. Seasonal and interannual dynamics of polyphenols in Myriophyllum verticillatum and their allelopathic activity on Anabaena variabilis. Aquatic Botany 91: 110–116.

    Article  CAS  Google Scholar 

  • Bolser, R. C. & M. E. Hay, 1998. A field test of inducible resistance to specialist and generalist herbivores using the water lily Nuphar luteum. Oecologia 116: 143–153.

    Article  PubMed  Google Scholar 

  • Brönmark, C., T. Lakowitz & J. Hollander, 2011. Predator-induced morphological plasticity across local populations of a freshwater snail. PLoS ONE 6(7): e21773.

    Article  PubMed  PubMed Central  Google Scholar 

  • Celewicz-Goldyn, S., 2010. Influence of Ceratophyllum demersum L. on phytoplankton structure in a shallow eutrophic lake. Oceanological and Hydrobiological Studies 39(3): 121–128.

    Article  Google Scholar 

  • Claessen, D., D. E. Rozen, O. P. Kuipers, L. Sogaard-Andersen & G. P. van Wezel, 2014. Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nature Review Microbiology 12: 115–124.

    Article  CAS  Google Scholar 

  • De Philippis, R. & M. Vincenzini, 1998. Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiology Reviews 22: 151–175.

    Article  Google Scholar 

  • De Philippis, R., M. C. Margheri, R. Materassi & M. Vincenzini, 1998. Potential of unicellular cyanobacteria from saline environments as exopolysaccharide producers. Applied and Environmental Microbiology 64(3): 1130–1132.

    PubMed  PubMed Central  Google Scholar 

  • Dong, J., J. J. Lu, G. B. Li & L. R. Song, 2013. Influences of a submerged macrophyte on colony formation and growth of a green alga. Aquatic Biology 19(5): 265–274.

    Article  Google Scholar 

  • Dunker, S., J. Althammer, G. Pohnert & C. Wilhelm, 2017. A fateful meeting of two phytoplankton species-chemical vs. cell-cell-interactions in co-cultures of the green algae Oocystis marssonii and the Cyanobacterium Microcystis aeruginosa. Microbial Ecology. doi:10.1007/s00248-016-0927-1.

  • Erhard, D. & E. M. Gross, 2006. Allelopathic activity of Elodea Canadensis and Elodea nuttallii against epiphytes and phytoplankton. Aquaic Botany 85: 203–211.

    Article  Google Scholar 

  • Fisher, R. M., T. Bel & S. A. West, 2016. Multicellular group formation in response to predators in the algae Chlorella vulgaris. Journal of Evolutionary Biology 29: 551–559.

    Article  CAS  PubMed  Google Scholar 

  • Gross, E. M., D. Erhard & I. Enikö, 2003. Allelopathic activity of Ceratophyllum demersum L. and Najas marina spp. Intermedia (Wolfgang) Casper. Hydrobiologia 506–509(1–3): 583–589.

    Article  Google Scholar 

  • He, F., P. Deng, X. H. Wu, S. P. Cheng, Y. N. Gao & Z. B. Wu, 2008. Allelopathic effects on Scenedesmus obliquus by two submerged macrophytes Najas minor and Potamogeton malaianus. Fresenius Environmental Bulletin 17(1): 92–97.

    CAS  Google Scholar 

  • Hessen, D. O. & E. Van Donk, 1993. Morphological changes in Scenedesmus induced by substances released from Daphnia. Archiv fur Hydrobologie 127: 129–140.

    Google Scholar 

  • Hilt, S., M. Ghobrial & E. M. Gross, 2006. In situ allelopathic potential of Myriophyllum verticillatum (Haloragaceae) against selected phytoplankton species. Journal of Phycology 42: 1189–1198.

    Article  Google Scholar 

  • Hu, H. Y. & Y. Hong, 2008. Algal-bloom control by allelopathy of aquatic macrophytes-a review. Frontiers of Environmental Science & Engineering in China 2: 421–438.

    Article  Google Scholar 

  • Jeffries, M., 1990. Evidence of induced plant defences in a pondweed. Freshwater Biology 23: 265–269.

    Article  Google Scholar 

  • Kleiven, S. & W. Szczepanska, 1988. The effects of extracts from Chara tomentosa and two other aquatic macrophytes on seed germination. Aquatic Botany 32: 193–198.

    Article  Google Scholar 

  • Kroen, W. K. & W. R. Rayburn, 1984. Influence of growth status and nutrients on extracellular polysaccharide synthesis by the soil alga Chlamydomonas mexicana (Chlorophyceae). Journal of Phycology 20(2): 253–257.

    Article  CAS  Google Scholar 

  • Leflaive, J., G. Lacroix, Y. Nicaise & L. Ten-Hage, 2008. Colony induction and growth inhibition in Desmodesmus quadrispina (Chlorococcales) by allelochemicals released from the filamentous alga Uronema confervicolum (Ulotrichales). Environmental Microbiology 10(6): 1536–1546.

    Article  CAS  PubMed  Google Scholar 

  • Leu, E., A. K. Liszkay, C. Goussias & E. M. Gross, 2002. Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum inhibit photosystem II. Plant Physiology 130: 2011–2018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H. S., Q. Sun, S. J. Zhao, et al., 2000. The experiment principle and technique on plant physiology and biochemistry. Higher Education Press, Beijing: 194–197.

    Google Scholar 

  • Lichtenthaler, H. K. & C. Buschmann, 2001. Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. In Wrolstad, R. E., T. E. Acree, H. An, E. A. Decker, M. H. Penner, D. S. Reid, S. J. Schwartz, C. F. Shoemaker & P. Sporns (eds.), Current Protocols in Food Analytical Chemistry. Wiley, London: F 4.3.1–F 4.3.8.

    Google Scholar 

  • Lürling, M., 2009. Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Annales de Limnologie - International Journal of Limnology 39: 85–101.

    Article  Google Scholar 

  • Lurling, M. & E. Van Donk, 1996. Zooplankton-induced unicell-colony transformation in Scenedesmus acutus and its effect on growth of herbivore Daphnia. Oecologia 108: 432–437.

    Article  PubMed  Google Scholar 

  • Lurling, M. & E. Van Donk, 1997. Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnology and Oceanography 42: 783–788.

    Article  Google Scholar 

  • Lurling, M. & E. Van Donk, 2000. Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88: 111–118.

    Article  Google Scholar 

  • Lurling, M., H. J. De Lange & E. Van Donk, 1997. Changes in food quality of the green alga Scenedesmus induced by Daphnia infochemicals: biochemical composition and morphology. Freshwater Biology 38: 619–628.

    Article  CAS  Google Scholar 

  • Lürling, M., G. Van Geest & M. Scheffer, 2006. Importance of nutrient competition and allelopathic effects in suppression of the green alga Scenedesmus obliquus by the macrophytes Chara, Elodea and Myriophyllum. Hydrobiologia 556: 209–220.

    Article  Google Scholar 

  • Mayeli, S. M., S. Nandini & S. S. S. Sarma, 2005. The efficacy of Scenedesmus morphology as a defense mechanism against grazing by selected species of rotifers and cladocerans. Aquatic Ecology 38: 515–524.

    Article  Google Scholar 

  • Mello, M. M. E., M. C. S. Soares, F. Roland & M. Lürling, 2012. Growth of inhibition and colony formation in the cyanobacterium Microcystis aeruginosa induced by the cyanobacterium Cylindrospermopsis raciborskii. Journal of Plankton Research 34(11): 987–994.

    Article  Google Scholar 

  • Mohamed, Z. A., 2017. Macrophytes-cyanobacteria allelopathic interactions and their implications for water resources management- a review. Limnologica 63: 122–132.

    Article  CAS  Google Scholar 

  • Moreno, J., M. A. Vargas, H. Olivares, J. Rivas & M. G. Guerrero, 1998. Exopolysaccharide production by the cyanobacterium Anabaena sp. ATCC 33047 in batch and continuous culture. Journal of Biotechnology 60(3): 175–182.

    Article  CAS  Google Scholar 

  • Mulderij, G., W. M. Mooij & E. Van Donk, 2005. Allelopathic growth inhibition and colony formation of the green alga Scenedesmus obliquus by the aquatic macrophate Stratiotes aloides. Aquatic Ecology 39(1): 11–21.

    Article  CAS  Google Scholar 

  • Mulderij, G., B. Mau, L. N. de Senerpont Domis, A. J. P. Smolders & E. Van Donk, 2009. Interaction between the macrophyte Stratiotes aloides and filamentous algae: does it indicate allelopathy? Aquatic Ecology 43: 305–312.

    Article  CAS  Google Scholar 

  • Nakai, S., Y. Inoue & M. Hosomi, 2000. Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Research 34: 3026–3032.

    Article  CAS  Google Scholar 

  • Nakai, S., S. Yamada & M. Hosomi, 2005. Anti-cyanobacterial fatty acids release from Myriophyllum spicatum. Hydrobiologia 543: 71–78.

    Article  CAS  Google Scholar 

  • Nakai, S., S. Asaoka, T. Okuda & W. Nishijima, 2014. Growth inhibition of Microcystis aeruginosa by allelopathic compounds originally isolated from Myriophyllum spicatum: temperature and light effects and evidence of possible major mechanisms. Journal of Chemical Engineering of Japan 47(6): 488–493.

    Article  CAS  Google Scholar 

  • O’donnell, D. R., S. B. Fey & K. L. Cottingham, 2013. Nutrient availability influences kairomone-induced defenses in Scenedesmus acutus (Chlorophyceae). Journal of Plankton Research 35: 191–200.

    Article  Google Scholar 

  • Otero, A. & M. Vincenzini, 2003. Extracellular polysaccharide synthesis by Nostoc strains as affected by N source and light intensity. Journal of Biotechnology 102(2): 143–152.

    Article  CAS  PubMed  Google Scholar 

  • Pakdel, F. M., L. Sim, J. Bearda & J. Davis, 2013. Allelopathic inhibition of microalgae by the freshwater stonewort, Chara australis, and a submerged angiosperm, Potamogeton crispus. Aquatic Botany 110: 24–30.

    Article  Google Scholar 

  • Pełechata, A. & M. Pełechaty, 2010. The in situ influence of Ceratophyllum demersum on a phytoplankton assemblage. Oceanological and Hydrobiological Studies 39: 95–101.

    Google Scholar 

  • Prusak, A. C., J. O’Neal & J. Kubanek, 2005. Prevalence of chemical defences among freshwater plants. Journal of Chemical Ecology 31: 1145–1160.

    Article  CAS  PubMed  Google Scholar 

  • Rangel, L. M., K. A. Ger, L. H. S. Silva, M. C. S. Soares, E. J. Faassen & M. Lürling, 2016. Toxicity overrides morphology on Cylindrospermopsis raciborskii grazing resistance to the calanoid copepod Eudiaptomus gracilis. Microbial Ecology 71: 835–844.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rausher, M. D., 2001. Co-evolution and plant resistance to natural enemies. Nature 411: 857–864.

    Article  CAS  PubMed  Google Scholar 

  • Rippka, R., R. Rippk, J. Deruelle, J. Waterbury, M. Herdman & R. Stanier, 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology 111: 1–61.

    Google Scholar 

  • Saito, K., M. Matsumoto, T. Sekine & J. Murakashi, 1989. Inhibitory substances from Myriophyllum brasiliense on growth of blue green algae. Journal of Natural Products 52: 1221–1226.

    Article  CAS  Google Scholar 

  • Schubert, L. E. & F. R. Trainor, 1974. Scenedesmus morphogenesis. Control of the unicell stage with phosphorus. British Phycological Journal 9: 1–7.

    Article  Google Scholar 

  • Shan, Y., Z. F. Wang, X. Z. Luo & Z. Zheng, 2015. Allelopathic inhibition effect of four aquatic macrophytes on Microcystis aeruginosa growth. Fresenius Environmental Bulletin 24(11B): 4025–4033.

    CAS  Google Scholar 

  • Staats, N., L. J. Stal & L. R. Mur, 2000. Exopolysaccharide production by the epipelic diatom Cylindrotheca closterium: effects of nutrient conditions. Journal of Experimental Marine Biology and Ecology 249(1): 13–27.

    Article  CAS  PubMed  Google Scholar 

  • Sun, X. M., Z. Y. Lu, B. Y. Liu, Q. H. Zhou, Y. Y. Zhang & Z. B. Wu, 2014. Allelopathic effects of pyrogallic acid secreted by submerged macrophytes on Microcystis aeruginosa: Role of ROS generation. Allelopathy Journal 33(1): 121–130.

    Google Scholar 

  • Svany, A., R. Paskauskas & S. Hilt, 2014. Effects of the allelopathically active macrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study. Hydrobiologia 737(1): 57–66.

    Article  Google Scholar 

  • Tang, K. W., 2003. Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): The role of a chemical signal. Journal of Plankton Research 25: 831–842.

    Article  Google Scholar 

  • Tollrian, R., 1995. Predator-induced morphological defences: costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76: 1691–1705.

    Article  Google Scholar 

  • Vanderstukken, M., S. A. J. Declerck, E. Decaestecker & K. Muylaert, 2014. Long-term allelopathic control of phytoplankton by the submerged macrophyte Elodea nuttallii. Freshwater Biology 59(5): 930–941.

    Article  Google Scholar 

  • Van Donk, E., A. Ianora & M. Vos, 2011. Induced defences in marine and freshwater phytoplankton: a review. Hydrobiologia 668: 3–19.

    Article  Google Scholar 

  • Wang, H. P., F. Liu, P. Luo, Z. H. Li, L. G. Zheng, H. Wang, D. S. Zou & J. S. Wu, 2017a. Allelopathic effects of Myriophyllum aquaticum on two cyanobacteria of Anabaena flos-aquae and Microcystis aeruginosa. Bulletin of Environmental Contamination and Toxicology 98: 556–561.

    Article  CAS  PubMed  Google Scholar 

  • Wang, L. C., J. M. Zi, R. B. Xu, S. Hilt, X. L. Hou & X. X. Chang, 2017b. Allelopathic effects of Microcystis aeruginosa on green algae and a diatom: evidence from exudates addition and co-culturing. Harmful Algae 61: 56–62.

    Article  Google Scholar 

  • West, S. A., R. M. Fisher, A. Gardner & T. E. Kiers, 2015. Major evolutionary transitions in individuality. Proceedings of the National Academy of Sciences of the United States of America 112(3): 10112–10119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xian, Q. M., H. D. Chen, H. X. Zhou & D. Q. Yin, 2007. Allelopathic activity and nutrient competition between Ceratophyllum demersum and Microcystis aeruginosa. Allelopathy Journal 19(1): 227–232.

    Google Scholar 

  • Yang, Z. & F. X. Kong, 2012. Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas sp. Journal of Limnology 71(1): 61–66.

    Article  CAS  Google Scholar 

  • Yang, Z., F. X. Kong, M. Zhang, Z. Yang, Y. Yu & S. Q. Qian, 2009. Effect of filtered cultures of flagellate Ochromonas sp. on colony formation in Microcystis aeruginosa. International Review of Hydrobiology 94(2): 143–152.

    Article  CAS  Google Scholar 

  • Zhang, S. H., S. P. Cheng, H. Q. Wang, F. He & Z. B. Wu, 2009. Allelopathic interactions between the Potamogeton spp. and toxic cyanobacteria (Microcystis aeruginosa). Alellopathy Journal 23: 379–390.

    Google Scholar 

  • Zhang, T. T., M. He, A. P. Wu & L. W. Nie, 2012. Inhibitory effects and mechanisms of Hydrilla verticillata (Linn.f.) Royle extracts on freshwater algae. Bulletin of Environmental Contamination and Toxicology 88: 477–481.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, J. G., F. F. He, Z. H. Chen, H. J. Li, J. M. Hu & F. P. Liu, 2012. Effect of culture and extract solutions of macrophytes on the growth of three common algae. Journal of Freshwater Ecology 27: 367–379.

    Article  Google Scholar 

  • Zheng, G. L., R. B. Xu, X. X. Chang, S. Hilt & C. Wu, 2013. Cyanobacteria can allelopathically inhibit submerged macrophytes: effects of Microcystis aeruginosa extracts and exudates on Potamogeton malaianus. Aquatic Botany 109: 1–7.

    Article  CAS  Google Scholar 

  • Zhu, X. X., J. Wang, Q. W. Chen, G. Chen, Y. Huang & Z. Yang, 2016. Costs and trade-offs of grazer induced defenses in Scenedesmus under deficient resource. Scientific Reports 6: 22594.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuo, S. P., Z. S. Fang, S. Y. Yang, K. Wan & Y. J. Han, 2015. Effect of allelopathic potential from selected aquatic macrophytes on algal interaction in the polluted water. Biochemical Systematics and Ecology 61: 133–138.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation Project of China (no. 31500380) and Dr. Start-up Foundation Project of Henan Normal University (no. qd14183) and Key Scientific & Technological Project of Henan Province (No. 152102310314). We really feel quite grateful and thankful for the editors and two anonymous reviewers’ suggestions in improving the whole manuscript.

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  1. College of Fisheries, Henan Normal University, Jianshe Road, Xinxiang, 453007, Henan, China

    Jing Dong, Yunni Gao, Mengyang Chang, Hanhui Ma, Kun Han, Xin Tao & Yan Li

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  1. Jing Dong
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  2. Yunni Gao
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  3. Mengyang Chang
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  4. Hanhui Ma
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Correspondence to Jing Dong.

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Dong, J., Gao, Y., Chang, M. et al. Colony formation by the green alga Chlorella vulgaris in response to the competitor Ceratophyllum demersum . Hydrobiologia 805, 177–187 (2018). https://doi.org/10.1007/s10750-017-3294-0

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