Abstract
In aquatic ecosystems, many phytoplankton species have evolved various inducible defense mechanisms against the predation. The expression of these defenses is affected by environmental conditions such as nutrient availability. Here, we investigated the anti-grazer colony formation in Scenedesmus obliquus at different magnesium concentrations (0–7.3 mg L−1 Mg2+) in the presence of zooplankton (Daphnia)-derived infochemicals. Results showed that at adequate Mg2+, S. obliquus formed high proportions of multi-celled (e.g., four- and eight-celled) colonies, resulting in significantly increased number of cells per colony in response to Daphnia filtrate. On the other hand, in Mg2+-deficient treatment, the proportion of multi-celled colonies decreased, together with reduced algal growth rate and photosynthetic efficiency. Finally, the treatment without Mg2+ strongly suppressed the formation of large colony (mainly eight-celled colonies), whereas the algal growth rate was comparable to that in Mg2+ sufficient treatment. Despite the inhibition of colony formation, the time reaching the maximum number of cells per colony was not affected by the Mg2+ concentration, which generally took three days in all groups. Our results indicate that Mg2+ deficient/absent environments significantly reduced anti-grazing colony formation but not the algal growth, suggesting strong dependability of this morphological defensive trait to magnesium fluctuation in S. obliquus.
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References
Esakkimuthu S, Krishnamurthy V, Govindarajan R, Swaminathan K (2016) Augmentation and starvation of calcium, magnesium, phosphate on lipid production of Scenedesmus obliquus. Biomass Bioenergy 88:126–134
Farhat N, Elkhouni A, Zorrig W, Smaoui A, Abdelly C, Rabhi M (2016) Effects of magnesium deficiency on photosynthesis and carbohydrate partitioning. Acta Physiol Plant 38:145
Hansson M, Lundqvist J, Sirijovski N, Al-Karadaghi S, Subunits IMC (2014) Magnesium chelatase: the molecular motor of chlorophyll biosynthesis. Science 28:41–84
Hessen DO, Van Donk E (1993) Morphological changes in Scenedesmus induced by substances released from Daphnia. Arch Hydrobiol 127:129–129
Huang Y, Nan HH, Zhu XX, Li BP, Zhang Z, Yang Z (2016) Waterborne copper impairs grazer-induced colony formation and photosynthetic efficiency in Scenedesmus obliquus. Limnol Oceanogr 61:625–634
Huang Y, Cui GL, Li BP, Zhu XX, Yang Z (2018) Elevated atmospheric CO2 enhances grazer-induced morphological defense in the freshwater green alga Scenedesmus obliquus. Limnol Oceanogr 63:1004–1014
Karley AJ, White PJ (2009) Moving cationic minerals to edible tissues: potassium, magnesium, calcium. Curr Opin Plant Biol 12:291–298
Kiørboe T (1993) Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Adv Mar Biol 29:1–72
Kiørboe T (2011) How zooplankton feed: mechanisms, traits and trade-offs. Biol Rev 86:311–339
Knoop V, Groth-Malonek M, Gebert M, Eifler K, Weyand K (2005) Transport of magnesium and other divalent cations: evolution of the 2-TM-GxN proteins in the MIT superfamily. Mol Gen Genomics 274:205–216
Kobayashi NI, Saito T, Iwata N, Ohmae Y, Iwata R, Tanoi K, Nakanishi TM (2013) Leaf senescence in rice due to magnesium deficiency mediated defect in transpiration rate before sugar accumulation and chlorosis. Physiol Plantarum 148:490–501
Lampert W, Rothhaupt KO, Von Elert E (1994) Chemical induction of colony formation in a green alga (Scenedesmus acutus) by grazers (Daphnia). Limnol Oceanogr 39: 1543–1550
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Analysis 4:142–196
Long JD, Smalley GW, Barsby T, Anderson JT, Hay ME (2007) Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton. P Natl Acad Sci USA 104:10512–10517
Lürling M (2003) Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Ann Limnol -Int J Lim 39:85–101
Lürling M, Van Donk E (1996) Zooplankton-induced unicell-colony transformation in Scenedesmus acutus and its effect on growth of herbivore Daphnia. Oecologia 108:432–437
Lürling M, Van Donk E (1997) Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnol Oceanogr 42:783–788
Lürling M, Van Donk E (1999) Grazer-induced colony formation in Scenedesmus acutus (Chlorophyceae): ecomorph expression at different temperatures. J Phycol 35:1120–1126
Lürling M, Van Donk E (2000) Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos 88:111–118
Lürling M, De Lange HJ, Van Donk E (1997) Changes in food quality of the green alga Scenedesmus induced by Daphnia infochemicals: biochemical composition and morphology. Freshw Biol 38:619–628
Mayeli SM, Nandini S, Sarma SSS (2005) The efficacy of Scenedesmus morphology as a defense mechanism against grazing by selected species of rotifers and cladocerans. Aquat Ecol 38:515–524
Mengel K, Kirkby EA (1978) Principles of plant nutrition. International Potash Institutes, Bern
O'Donnell DR, Fey SB, Cottingham KL (2012) Nutrient availability influences kairomone-induced defenses in Scenedesmus acutus (Chlorophyceae). J Plankton Res 35:191–200
Pan Y, Liu C, Li F, Zhou CQ, Yan SW, Dong JY, Li TR, Duan CQ (2017) Norfloxacin disrupts Daphnia magna-induced colony formation in Scenedesmus quadricauda and facilitates grazing. Ecol Eng 102:255–261
Pančić M, Kiørboe T (2018) Phytoplankton defence mechanisms: traits and trade-offs. Biol Rev 93:1269–1303
Ploug H, Stolte W, Epping E, Jorgensen BB (1999) Diffusive boundary layers, photosynthesis, and respiration of the colony-forming plankton algae, Phaeocystis sp. Limnol Oceanogr 44:1949–1958
Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:307–321
Smetacek V, Assmy P, Henjes J (2004) The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles. Antarct Sci 16:541–558
Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J Plankton Res 25:831–842
Tang N, Li Y, Chen LS (2012) Magnesium deficiency–induced impairment of photosynthesis in leaves of fruiting Citrus reticulata trees accompanied by up-regulation of antioxidant metabolism to avoid photo-oxidative damage. J Plant Nutr Soil Sci 175:784–793
Thornton D (2002) Diatom aggregation in the sea: mechanisms and ecological implications. Eur J Phycol 37:149–161
Van Donk E, Ianora A, Vos M (2011) Induced defences in marine and freshwater phytoplankton: a review. Hydrobiologia 668(1):3–19
Verbruggen N, Hermans C (2013) Physiological and molecular responses to magnesium nutritional imbalance in plants. Plant Soil 368:87–99
Wu XY, Zhang J, Qin BL, Cui GL, Yang Z (2013) Grazer density-dependent response of induced colony formation of Scenedesmus obliquus to grazing-associated infochemicals. Biochem Syst Ecol 50:286–292
Yang Z, Kong FX (2012) Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas sp. J Limnol 71:61–66
Yang Z, Kong FX, Shi XL, Xing P, Zhang M (2007) Effects of Daphnia-associated infochemicals on the morphology, polysaccharides content and PSII-efficiency in Scenedesmus obliquus. Int Rev Hydrobiol 92:618–625
Yang Z, Kong FX, Shi XL, Zhang M, Xing P, Cao HS (2008) Changes in the morphology and polysaccharide content of Microcystis aeruginosa (cyanobacteria) during flagellate grazing. J Phycol 44:716–720
Yang GH, Yang LT, Jiang HX, Li Y, Wang P, Chen LS (2012) Physiological impacts of magnesium-deficiency in Citrus seedlings: photosynthesis, antioxidant system and carbohydrates. Trees 26:1237–1250
Yang JW, Li BP, Zhang CW, Luo HX, Yang Z (2016) pH-associated changes in induced colony formation and growth of Scenedesmus obliquus. Fund Appl Limnol 187:241–246
Yasumoto K, Nishigami A, Kasai F, Kusumi T, Ooi T (2006) Isolation and absolute configuration determination of aliphatic sulfates as the Daphnia kairomones inducing morphological defense of a phytoplankton. Chem Pharm Bull 54:271–274
Yasumoto K, Nishigami A, Aoi H, Tsuchihashi C, Kasai F, Kusumi T, Ooi T (2008) Isolation of new aliphatic sulfates and sulfamate as the Daphnia kairomones inducing morphological change of a phytoplankton Scenedesmus gutwinskii. Chem Pharm Bull 56:133–136
Zhu XX, Wang J, Lu YC, Chen QW, Yang Z (2015a) Grazer-induced morphological defense in Scenedesmus obliquus is affected by competition against Microcystis aeruginosa. Sci Rep 5:12743
Zhu XX, Wu XY, Zhang L, Zhu C, Yang Z (2015b) Response of grazer-induced colony formation of Scenedesmus obliquus in relation to grazer’s size. Fund Appl Limnol 186:243–248
Zhu XX, Yang JW, Xu N, Chen G, Yang Z (2015c) Combined effects of nitrogen concentrations and Daphnia culture filtrate on colony size of Scenedesmus obliquus. Algal Res 9:94–98
Zhu XX, Wang J, Chen QW, Chen G, Huang Y, Yang Z (2016) Costs and trade-offs of grazer-induced defenses in Scenedesmus under deficient resource. Sci Rep 6:22594
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We greatly appreciate the two anonymous reviewers for their constructive comments.
Funding
This study was supported by the National Natural Science Foundation of China (31470508), Natural Science Youth Foundation of Jiangsu Province (BK20150972), “333 High Concentration Talent Project” in Jiangsu Province (BRA2017452), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.
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Hou, X., Zhou, Q., Wang, Z. et al. Magnesium depletion suppresses the anti-grazer colony formation in Scenedesmus obliquus. Environ Sci Pollut Res 25, 34228–34235 (2018). https://doi.org/10.1007/s11356-018-3191-8
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DOI: https://doi.org/10.1007/s11356-018-3191-8