Interactive Effects of Temperature, Nitrogen, and Zooplankton on Growth and Protein and Carbohydrate Content of Cyanobacteria from Western Lake Erie


Harmful algal blooms (HABs) in freshwater ecosystems, especially of cyanobacterial species, are becoming more frequent and expanding geographically, including in Lake Erie in North America. HABs are the result of complex and synergistic environmental factors, though N or P eutrophication is a leading cause. With global mean temperatures expected to increase an additional 2°C - 5°C by 2100, cyanobacterial blooms are predicted to increase even more, given their typically-high temperature optimum for growth. We investigated how increases in temperature and nitrogen, singly or in combination, affect the growth, food quality, and herbivory of Lake Erie cyanobacteria. Algal community samples collected from Lake Erie, and isolated non-N-fixing (Microcystis aeruginosa) and N-fixing (Anabaena flos-aquae) cyanobacterial species, were cultured at 20°C, 25°C, or 30°C, and at 5, 50, 150, or 250 μM N, and then analyzed for growth and (for isolates) content of total protein and non-structural carbohydrates (NSC). Temperature and N both affected algal growth, and there were temperature × N interactions, which were sometimes affected by presence/absence of zooplankton. For example, cyanobacteria (but not green algae) growth increased with both temperature and N, especially from 25°C to 30°C, but N and herbivore presence increased cyanobacterial growth primarily only at 30°C. In general, temperature and N had little consistent effect on NSC, but increasing temperature and N tended to increase protein content in Microcystis and Anabaena (temperature effects mostly at higher N levels). In Anabaena, increases in N did not increase growth or protein at 20°C or 25°C, but did increase both at 30°C, indicating that N fixation is damaged at high temperatures and that high NO3 can overcome this damage. These results indicate that future global warming and continued eutrophication will increase cyanobacterial growth, as well influence algal herbivory and competition between N-fixing and non-N-fixing cyanobacteria.

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Bista, D. , Heckathorn, S. , Bridgeman, T. , Chaffin, J. and Mishra, S. (2014) Interactive Effects of Temperature, Nitrogen, and Zooplankton on Growth and Protein and Carbohydrate Content of Cyanobacteria from Western Lake Erie. Journal of Water Resource and Protection, 6, 1139-1153. doi: 10.4236/jwarp.2014.612106.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Paerl, H.W. and Huisman, J. (2008) Blooms Like It Hot. Science, 320, 57-58.
[2] Paerl, H.W. and Paul, V.J. (2012) Climate Change: Links to Global Expansion of Harmful Cyanobacteria. Water Research, 46, 1349-1363.
[3] Havens, K.E., Fukushima, T., Xie, P., Iwakuma, T., James, R. T., Takamura, N., Hanazato, T. and Yamamoto, T. (2001) Nutrient Dynamics and the Eutrophication of Shallow Lakes Kasumigaura (Japan), Donghu (PR China), and Okeechobee (USA). Environmental Pollution, 111, 263-272.
[4] Qin, B., Zhu, G., Gao, G., Zhang, Y., Li, W., Paerl, H.W. and Carmichael, W.W. (2010) A Drinking Water Crisis in Lake Taihu, China: Linkage to Climatic Variability and Lake Management. Environmental Management, 45, 105-112.
[5] Conley, D.J., Bonsdorff, E., Carstensen, J., Destouni, G., Gustafsson, B.G., Hansson, L.A., Rabalais, N.N, Voss, M. and Zillen, L. (2009) Tackling Hypoxia in the Baltic Sea: Is Engineering a Solution? Environmental Science and Technology, 43, 3407-3411.
[6] Dodds, W.K., Bouska W.W., Eitzmann, J.L., Pilger, T.J., Pitts, K.L., Riley, A.J., Schloesser, J.T. and Thornbrugh, D.J. (2009) Eutrophication of U.S. Freshwaters: Analysis of Potential Economic Damages. Environmental Science and Technology, 43, 12-19.
[7] Sarnelle, O., Gustafsson, S. and Hansson, L.A. (2009) Effects of Cyanobacteria on Fitness Components of the Herbivore Daphnia. Journal of Plankton Research, 32, 471-477.
[8] Paerl, H.W. (2008) Nutrient and Other Environmental Controls of Harmful Cyanobacterial Blooms along the Freshwater-Marine Continuum. In: Hudnell, K.H., Ed., Cyanobacterial Harmful Algal Blooms: State of the Science Research Needs Series: Advances in Experimental Medicine and Biology, Vol. 619, Springer, New York, 217-237.
[9] Gilbert, J.J. and Claska, M.E. (1998) The Effect of Temperature on the Response of Daphnia to Toxic Cyanobacteria. Freshwater Biology, 39, 221-232.
[10] Turner, T.J. and Tester, P.A. (1997) Toxic Marine Phytoplankton, Zooplankton Grazers, and Pelagic Food Webs. Limnology and Oceanography, 42, 1203-1214.
[11] Johnk, K.D., Huisman, J., Sharples, J., Sommeijer, B., Visser, P.M. and Stroom, J.M. (2008) Summer Heat Waves Promote Blooms of Harmful Cyanobacteria. Global Change Biology, 14, 495-512.
[12] Wilhelm, S. and Adrian, R. (2008) Impact of Summer Warming on the Thermal Characteristics of a Polymictic Lake and Consequences for Oxygen, Nutrients and Phytoplankton. Freshwater Biology, 53, 226-237.
[13] Sommer, U. (1984) The Paradox of the Plankton: Fluctuations of Phosphorus Availability Maintain Diversity of Phytoplankton in Flow-through Cultures. Limnology and Oceanography, 29, 633-636.
[14] Rapala, J., Sivonen, K., Lyra, C. and Niemela, S.I. (1997) Variation of Microcystins, Cyanobacterial Hepatotoxins, in Anabaena spp. as a Function of Growth Stimulation. Applied and Environmental Microbiology, 63, 2206-2212.
[15] Oliver, R.L. and Ganf, G.G. (2000) Freshwater Blooms. In: Whitton, B.A. and Potts, M., Eds., The Ecology of Cyanobacteria, Their Diversity in Time and Space, Kluwer Academic, Dordrecht, 149-194.
[16] Paerl, H.W., Fulton, R.S., Moisander, P.H. and Dyble, J. (2001) Harmful Freshwater Algal Blooms, with an Emphasis on Cyanobacteria. The Scientific World Journal, 1, 76-113.
[17] Vitousek, P., Aber, J., Howarth, R., Likens, G., Matson, P., Schindler, D., Schlesinger, W. and Tilman, D. (1997) Human Alteration of the Global N Cycle: Causes and Consequences. Issues in Ecology, 1, 1-17.
[18] Carpenter, S.R., Caraco, N.F., Correll, D.L., Howarth, R.W., Sharpley, A.N. and Smith, V.H. (1998) Nonpoint Pollution of Surface Waters with Phosphorus and Nitrogen. Ecological Applications, 8, 559-568.[0559:NPOSWW]2.0.CO;2
[19] Paerl, H.W. and Scott, J.T. (2010) Throwing Fuel on the Fire: Synergistic Effects of Excessive Nitrogen Inputs and Global Warming on Harmful Algal Blooms. Environmental Science and Technology, 44, 7756-7758.
[20] Trimbee, A.M. and Prepas, E.E. (1987) Evaluation of Total Phosphorus as a Predictor of Relative Biomass of Blue-Green Algae with an Emphasis on Alberta Lakes. Canadian Journal of Fisheries and Aquatic Sciences, 44, 1337-1342.
[21] Watson, S.B., McCauley, E. and Downing, J.A. (1997) Patterns in Phytoplankton Taxonomic Composition across Temperate Lakes of Differing Nutrient Status. Limnology and Oceanography, 42, 487-495.
[22] Chaffin, J., Bridgeman, T. and Bade, D. (2013) Nitrogen Constrains the Growth of Late Summer Cyanobacterial Blooms in Lake Erie. Advances in Microbiology, 3, 16-26.
[23] Codd, G.A. and Poon, G.K. (1988) Cyanobacterial Toxins. In: Rogers, L.J. and Gallon, J.R., Eds., Biochemistry of the Algae and Cyanobacteria, Clarendon Press, Oxford, 283-296.
[24] Dokulil, M.T. and Teubner, K. (2000) Cyanobacterial Dominance in Lakes. Hydrobiologia, 438, 1-12.
[25] Chaffin, J.D., Bridgeman, T.B., Heckathorn, S.A. and Mishra, S. (2011) Assessment of Microcystis Growth Rate Potential and Nutrient Status across a Trophic Gradient in Western Lake Erie. Journal of Great Lakes Research, 37, 92-100.
[26] Orr, P.T. and Jones, G.J. (1998) Relationship between Microcystin Production and Cell Division Rates in Nitrogen-Limited Microcystis aeruginosa Cultures. Limnology and Oceanography, 43, 1604-1614.
[27] Watanabe, M.F. and Oishi, S. (1985) Effects of Environmental Factors on Toxicity of a Cyanobacterium (Microcystis aeruginosa) under Culture Conditions. Applied and Environmental Microbiology, 49, 1342-1344.
[28] Vezie, C., Rapala, J., Vaitomaa, J., Seitsonen, J. and Sivonen, K. (2002) Effect of Nitrogen and Phosphorus on Growth of Toxic and Nontoxic Microcystis Strains and on Intracellular Microcystin Concentrations. Microbial Ecology, 43, 443-454.
[29] Kay, R.A. and Barton, L.L. (1991) Microalgae as Food and Supplement. Critical Reviews in Food Science and Nutrition, 30, 555-573.
[30] Hitchcock, G.L. (1980) Diel Variation in Chlorophyll α, Carbohydrate and Protein Content of the Marine Diatom Skeletonema costatum. Marine Biology, 57, 271-278.
[31] IPCC (2007) A Report of Working Group I of the Intergovernmental Panel on Climate Change. Summary for Policymakers and Technical Summary.
[32] Canale, R.P. and Vogel, A.H. (1974) Effects of Temperature on Phytoplankton Growth. Journal of the Environmental Engineering Division, 100, 229-241.
[33] Paul, V.J. (2008) Global Warming and Cyanobacterial Harmful Algal Blooms. In: Hudnell, K.H., Ed., Cyanobacterial Harmful Algal Blooms: State of the Science Research Needs Series: Advances in Experimental Medicine and Biology, Vol. 619, Springer, New York, 239-257.
[34] Takamura, N., Iwakuma, T. and Yasuno, M. (1985) Photosynthesis and Primary Production of Microcystis aeruginosa Kütz in Lake Kasumigaura. Journal of Plankton Research, 7, 303-312.
[35] Robarts, R.D. and Zohary, T. (1987) Temperature Effects on Photosynthetic Capacity, Respiration, and Growth Rates of Bloom-Forming Cyanobacteria. New Zealand Journal of Marine and Freshwater Research, 21, 391-399.
[36] Reynolds, C.S. (2006) Ecology of Phytoplankton. Cambridge University Press, Cambridge.
[37] Sivonen, K. (1990) Effects of Light, Temperature, Nitrate, Orthophosphate, and Bacteria on Growth of and Hepatotoxin Production by Oscillatoria agardhii Strains. Applied and Environmental Microbiology, 56, 2658-2666.
[38] Renaud, S.M., Thinh, L.V., Lambrinidis, G. and Parry, D.L. (2002) Effect of Temperature on Growth, Chemical Composition and Fatty Acid Composition of Tropical Australian Microalgae Grown in Batch Cultures. Aquaculture, 211, 195-214.
[39] Bridgeman, T.B., Chaffin, J.D. and Filbrun, J.E. (2013) A Novel Method for Tracking Western Lake Erie Microcystis Blooms, 2002-2011. Journal of Great Lakes Research, 39, 83-89.
[40] Stumpf, R.P., Wynne, T.T., Baker, D.B. and Fahnenstiel, G.L. (2012) Interannual Variability of Cyanobacterial Blooms in Lake Erie. PLoS ONE, 7, e42444.
[41] Guillard, R.R.L. and Lorenzen, C.J. (1972) Yellow-Green Algae with Chlorophyllidec. Journal of Phycology, 8, 10-14.
[42] Bista, D.R. (2012) Effect of Increased Temperature and Nitrogen on the Non-N-fixing vs. N-Fixing Cyanobacteria in Western Lake Erie: Implications for Competition and Climate Change. M.Sc. Disertation, University of Toledo, Toledo.
[43] Barnes, J.D., Balaguer, L., Manrique, E., Elvira, S. and Davison, A.W. (1992) A Reappraisal of the Use of DMSO for the Extraction and Determination of Chlorophylls a and b in Lichens and Higher Plants. Environmental and Experimental Botany, 32, 85-100.
[44] Seely, G.R., Ducan, M.J. and Vidaver, W.E. (1972) Preparative and Analytical Extraction of Pigments from Brown Algae with Dimethyl Sulfoxide. Marine Biology, 12, 184-188.
[45] Chaffin, J., Bridgeman, T., Heckathorn, S.A. and Krause, A. (2012) Role of Suspended Sediments and Mixing in Reducing Photoinhibition in the Bloom-Forming Cyanobacterium Microcystis. Journal of Water Resource and Protection, 4, 1029-1041.
[46] Furuki, T., Maeda, S., Imajo, S., Hiroi, T., Amaya, T., Hirokawa, T., Ito, K. and Nozawa, H. (2003) Rapid and Selective Extraction of Phycocyanin from Spirulina platensis with Ultrasonic Cell Disruption. Journal of Applied Phycology, 15, 319-324.
[47] Sampath-Wiley, P. and Neefus, C.D. (2007) An Improved Method for Estimating R-Phycoerythrin and R-Phycocyanin Contents from Crude Aqueous Extracts of Porphyra (Bangiales, Rhodophyta). Journal of Applied Phycology, 19, 123-129.
[48] Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. and Smith, F. (1956) Colorimetric Method for Determination of Sugars and Related Substances. Analytical Chemistry, 28, 350-356.
[49] Downing, T.G., Sember, C.S., Gehringer, M.M. and Leukes, W. (2005) Medium N:P Ratios and Specific Growth Rate Comodulate Microcystin and Protein Content in Microcystis aeruginosa PCC7806 and M. aeruginosa UV027. Microbial Ecology, 49, 468-473.
[50] Long, B.M., Jones, G.J. and Orr, P.T. (2001) Cellular Microcystin Content in N-Limited Microcystis aeruginosa Can Be Predicted from Growth Rate. Applied and Environmental Microbiology, 67, 278-283.
[51] Oh, H.M., Lee, S.J., Jang, M.H. and Yoon, B.D. (2000) Microcystin Production by Microcystis aeruginosa in a Phosphorus-Limited Chemostat. Applied and Environmental Microbiology, 66, 176-179.
[52] Mishra, S., Heckathorn, S.A., Barua, D., Wang, D., Joshi, P., Hamilton III, E.W. and Frantz, J. (2008) Interactive Effects of Elevated CO2 and Ozone on Leaf Thermotolerance in Field Grown Glycine max. Journal of Integrative Plant Biology, 50, 1396-1405.
[53] Ghosh, S., Gepstein, S., Heikkila, J.J. and Dumbroff, E.B. (1988) Use of a Scanning Densitometer or an ELISA Reader for Measurement of Nanogram Amount of Protein in Crude Extracts from Biological Tissue. Analytical Biochemistry, 169, 227-233.
[54] Tilman, D. (1982) Resource Competition and Community Structure. Princeton University Press, Princeton.
[55] Gilbert, J.J. and Claska, M.E. (1998) The Effect of Temperature on the Response of Daphnia to Toxic Cyanobacteria. Freshwater Biology, 39, 221-232.
[56] Tillmanns, A.R., Wilson, A.E., Pick, F.R. and Sarnelle, O. (2008) Meta-Analysis of Cyanobacterial Effects on Zooplankton Population Growth Rate: Species-Specific Responses. Fundamental and Applied Limnology, 171, 285-295.
[57] Wang, X., Qin, B., Gao, G. and Paerl, H.W. (2010) Nutrient Enrichment and Selective Predation by Zooplankton Promote Microcystis (Cyanobacteria) Bloom Formation. Journal of Plankton Research, 32, 457-470.
[58] Compaore, J. and Stal, L.J. (2010) Effect of Temperature on the Sensitivity of Nitrogenase to Oxygen in Two Heterocystous Cyanobacteria. Journal of Phycology, 46, 1172-1179.
[59] Marschner, H. (1995) Mineral Nutrition of Higher Plants. 2nd Edition, Academic Press, New York.
[60] Davis, T.W. and Gobler, C.J. (2011) Grazing by Mesozooplankton and Microzooplankton on Toxic and Non-Toxic Strains of Microcystis in the Transquaking River, a Tributary of Chesapeake Bay. Journal of Plankton Research, 33, 415-430.
[61] Ananadhi Padmanabhan, M.R., Annam Renita, A. and Stanley, S.A. (2010) Studies on the Effect of Nitrogen Source and the Growth of Marine Microalgae Algae. In: Recent Advances in Space Technology Services and Climate Change (RSTSCC), Chennai, 13-15 November 2010, 350-352.
[62] Hochachka, P.W. and Somero, G.N. (2002) Biochemical Adaptation, Mechanism and Process in Hysiological Evolution. Oxford University Press, New York.
[63] Song, L., Sano, T., Li, R., Makoto, W.M., Liu, Y.D. and Kaya, K. (1998) Microcystin Production of Microcystis viridis (cyanobacteria) under Different Culture Conditions. Phycological Research, 42, 19-23.
[64] Jacoby, J.M., Collier, D.C., Welch, E.B., Hardy, F.J. and Crayton, M. (2000) Environmental Factors Associated with a Toxic Bloom Microcystis aeruginosa. Canadian Journal of Fisheries and Aquatic Sciences, 57, 231-240.
[65] Sekadende, B.C., Lyimo, T.J. and Kurmayer, R. (2005) Microcystin Production by Cyanobacteria in the Mwanza Gulf (Lake Victoria, Tanzania). Hydrobiologia, 543, 299-304.
[66] Wu, S.K., Xie, P., Liang, G.D., Wang, S.B. and Liang, X.M. (2006) Relationships between Microcystins and Environmental Parameters in 30 Subtropical Shallow Lakes along the Yangtze River, China. Freshwater Biology, 51, 2309-2319.

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