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Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria

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Abstract

Rising temperatures are expected to favour the growth of bloom-forming cyanobacteria in temperate lakes, but may also change the composition of cyanobacterial communities. To predict future community and bloom dynamics, it is therefore important to understand how bloom-forming species respond to temperature. Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju is an invasive, toxin-producing, nitrogen-fixer that may benefit from warming. To understand how changing temperatures will influence its ability to compete against native North American bloom-formers, we characterized the thermal reaction norms and temperature traits of three C. raciborskii strains, four strains of Microcystis aeruginosa (Kützing) Kützing and one strain of Anabaena flos-aquae (Lyng.) Brèb. C. raciborskii strains had higher optimum temperatures and survived higher temperatures than toxic M. aeruginosa strains, but had no apparent advantage over the non-toxic M. aeruginosa strain or A. flos-aquae. M. aeruginosa strains and A. flos-aquae tolerated lower temperatures than C. raciborskii, suggesting that fitness differences at low temperature may be important in limiting the latter’s spread. Furthermore, we found that nutrient availability strongly influenced thermal reaction norm shape: nitrogen deprivation lowered growth rates and decreased both low- and high-temperature tolerance, but did not affect the optimum temperature in C. raciborskii.

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References

  • Barker, H. A., 1935. The culture and physiology of the marine dinoflagellates. Archiv für Mikrobiologie 6: 157–181.

    Article  Google Scholar 

  • Bonilla, S., L. Aubriot, M. C. S. Soares, M. González-Piana, A. Fabre, V. L. M. Huszar, M. Lürling, D. Antoniades, J. Padisák & C. Kruk, 2012. What drives the distribution of the bloom-forming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiology Ecology 79: 594–607.

    Article  CAS  PubMed  Google Scholar 

  • Boyd, P. W., T. A. Rynearson, E. A. Armstrong, F. Fu, K. Hayashi, Z. Hu, D. A. Hutchins, R. M. Kudela, E. Litchman, M. R. Mulholland, U. Passow, R. F. Strzepek, K. A. Whittaker, E. Yu & M. K. Thomas, 2013. Marine phytoplankton temperature versus growth responses from polar to tropical waters - Outcome of a scientific community-wide study. PLoS ONE 8: e63091.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Briand, J.-F., J.-F. Humbert, C. Leboulanger, C. Bernard & P. Dufour, 2004. Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? Journal of Phycology 40: 231–238.

    Article  Google Scholar 

  • Chapman, A. D. & C. L. Schelske, 1997. Recent appearance of Cylindrospermopsis in five hypereutrophic Florida lakes. Journal of Phycology 33: 191–195.

    Article  Google Scholar 

  • Chonudomkul, D., W. Yongmanitchai, G. Theeragool, M. Kawachi, F. Kasai, K. Kaya & M. M. Watanabe, 2004. Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan. FEMS Microbiology Ecology 48: 345–355.

    Article  CAS  PubMed  Google Scholar 

  • Chorus, I. & J. Bartram, 1999. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring, and Management. E & FN Spon, London.

    Book  Google Scholar 

  • Chu, Z., X. Jin, N. Iwami & Y. Inamori, 2007. The effect of temperature on growth characteristics and competitions of Microcystis aeruginosa and Oscillatoria mougeotii in a shallow, eutrophic lake simulator system. Hydrobiologia 581: 217–223.

    Article  Google Scholar 

  • Conroy, J. D., E. L. Quinlan, D. D. Kane & D. A. Culver, 2007. Cylindrospermopsis in Lake Erie: testing its association with other cyanobacterial genera and major limnological parameters. Journal of Great Lakes Research 33: 519–535.

    Article  Google Scholar 

  • Dauta, A., J. Devaux, F. Piquemal & L. Boumnich, 1990. Growth rate of four freshwater algae in relation to light and temperature. Hydrobiologia 207: 221–226.

    Article  Google Scholar 

  • de Stasio, B. T., D. K. Hill, J. M. Kleinhans & N. P. Nibbelink, 1996. Potential effects of global climate change on small north-temperate lakes: physics, fish, and plankton. Limnology and Oceanography 41: 1136–1149.

    Article  Google Scholar 

  • Droop, M. R., 1973. Some thoughts on nutrient limitation in algae. Journal of Phycology 9: 264–272.

    CAS  Google Scholar 

  • Edwards, K. F., M. K. Thomas, C. A. Klausmeier & E. Litchman, 2015. Light and growth in marine phytoplankton: allometric, taxonomic, and environmental variation. Limnology and Oceanography 60: 540–552.

    Article  Google Scholar 

  • Figueredo, C. C., A. Giani & D. F. Bird, 2007. Does allelopathy contribute to Cylindrospermopsis raciborskii (Cyanobacteria) bloom occurrence and geographic expansion? Journal of Phycology 43: 256–265.

    Article  Google Scholar 

  • Fujimoto, N., R. Sudo, N. Sugiura & I. Yuhei, 1997. Nutrient-limited growth of Microcystis aeruginosa and Phormidium tenue and competition under various N:P supply ratios and temperatures. Limnology and Oceanography 42: 250–256.

    Article  CAS  Google Scholar 

  • Guillard, R. R. L., 1975. Culture of phytoplankton for feeding marine invertebrates. In Smith, W. L. & M. H. Chantey (eds), Culture of Marine Invertebrate Animals. Plenum Press, New York: 29–60.

    Chapter  Google Scholar 

  • Hong, Y., A. Steinman, B. Biddanda, R. Rediske & G. Fahnenstiel, 2006. Occurrence of the toxin-producing cyanobacterium Cylindrospermopsis raciborskii in Mona and Muskegon Lakes, Michigan. Journal of Great Lakes Research 32: 645–652.

    Article  Google Scholar 

  • Huisman, J., J. Sharples, J. M. Stroom, P. M. Visser, W. E. A. Kardinaal, J. M. H. Verspagen & B. Sommeijer, 2004. Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85: 2960–2970.

    Article  Google Scholar 

  • Imai, H., K.-H. Chang & S. Nakano, 2009. Growth responses of harmful algal species Microcystis (Cyanophyceae) under various environmental conditions. In Obayashi, Y., T. Isobe, A. Subramanian, S. Suzuki & S. Tanabe (eds), Interdisciplinary Studies on Environmental Chemistry – Environmental Research in Asia. Terrapub, Tokyo: 269–275.

    Google Scholar 

  • IPCC Fourth Assessment Report, 2007. Climate Change 2007: the physical science basis. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller (eds), Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.

    Google Scholar 

  • Isvánovics, V., H. M. Shafik, M. Présing & S. Juhos, 2000. Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshwater Biology 43: 257–275.

    Article  Google Scholar 

  • Jöhnk, K. D., P. M. Visser, J. Huisman, J. M. Stroom, J. Sharples & B. Sommeijer, 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology 14: 495–512.

    Article  Google Scholar 

  • Kahru, M., J. M. Leppanen & O. Rud, 1993. Cyanobacterial blooms cause heating of the sea surface. Marine Ecology Progress Series 101: 1–7.

    Article  Google Scholar 

  • Karentz, D. & T. J. Smayda, 1984. Temperature and seasonal occurrence patterns of 30 dominant phytoplankton species in Narragansett Bay over a 22-year period (1959–1980). Marine Ecology Progress Series 18: 277–293.

    Article  Google Scholar 

  • Kehoe, M., K. R. O. Brien, A. Grinham & M. A. Burford, 2015. Primary production of lake phytoplankton, dominated by the cyanobacterium Cylindrospermopsis raciborskii, in response to irradiance and temperature. Inland Waters 5: 93–10.

  • Kingsolver, J. G., 2009. The well-temperatured biologist. The American Naturalist 174: 755–768.

    Article  PubMed  Google Scholar 

  • Kling, H. J., 2009. Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria): a brief historic overview and recent discovery in the Assiniboine River (Canada). Fottea 9: 45–47.

    Article  Google Scholar 

  • Kormas, K. A., S. Gkelis, E. Vardaka & M. Moustaka-Gouni, 2011. Morphological and molecular analysis of bloom-forming Cyanobacteria in two eutrophic, shallow Mediterranean lakes. Limnologica 41: 167–173.

    Article  CAS  Google Scholar 

  • Kosten, S., V. L. M. Huszar, E. Bécares, L. S. Costa, E. van Donk, L.-A. Hansson, E. Jeppesen, C. Kruk, G. Lacerot, N. Mazzeo, L. de Meester, B. Moss, M. Lürling, T. Nõges, S. Romo & M. Scheffer, 2012. Warmer climates boost cyanobacterial dominance in shallow lakes. Global Change Biology 18: 118–126.

    Article  Google Scholar 

  • Litchman, E., 2000. Growth rates of phytoplankton under fluctuating light. Freshwater Biology 44: 223–235.

    Article  Google Scholar 

  • Litchman, E., 2010. Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecology Letters 13: 1560–1572.

    Article  PubMed  Google Scholar 

  • Litchman, E., P. de Tezanos Pinto, C. A. Klausmeier, M. K. Thomas & K. Yoshiyama, 2010. Linking traits to species diversity and community structure in phytoplankton. Hydrobiologia 653: 15–28.

    Article  CAS  Google Scholar 

  • Litchman, E., K. F. Edwards & C. A. Klausmeier, 2015. Microbial resource utilization traits and trade-offs: implications for community structure, functioning, and biogeochemical impacts at present and in the future. Frontiers in Microbiology 6: 254.

    Article  PubMed Central  PubMed  Google Scholar 

  • Lürling, M., F. Eshetu, E. J. Faassen, S. Kosten & V. L. M. Huszar, 2013. Comparison of cyanobacterial and green algal growth rates at different temperatures. Freshwater Biology 58: 552–559.

    Article  Google Scholar 

  • Magnuson, J. J., K. E. Webster, R. A. Assel, C. J. Bowser, P. J. Dillon, J. G. Eaton, H. E. Evans, E. J. Fee, R. I. Hall, L. R. Mortsch, D. W. Schindler & F. H. Quinn, 1997. Potential effects of climate changes on aquatic systems: Laurentian great lakes and Precambrian Shield region. Hydrological Processes 11: 825–871.

    Article  Google Scholar 

  • Marinho, M. M. & V. L. M. Huszar, 2002. Nutrient availability and physical conditions as controlling factors of phytoplankton composition and biomass in a tropical reservoir (Southeastern Brazil). Archiv für Hydrobiologie 153: 443–468.

    Google Scholar 

  • Martin, T. L. & R. B. Huey, 2008. Why “suboptimal” is optimal: Jensen’s inequality and ectotherm thermal preferences. The American Naturalist 171: E102–E118.

    Article  PubMed  Google Scholar 

  • Mehnert, G., F. Leunert, S. Cires, K. D. Jöhnk, J. Rucker, B. Nixdorf & C. Wiedner, 2010. Competitiveness of invasive and native cyanobacteria from temperate freshwaters under various light and temperature conditions. Journal of Plankton Research 32: 1009–1021.

    Article  CAS  Google Scholar 

  • Moisander, P. H., L. A. Cheshire, J. Braddy, E. S. Calandrino, M. Hoffman, M. F. Piehler & H. W. Paerl, 2012. Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability. FEMS Microbiology Ecology 79: 800–811.

    Article  CAS  PubMed  Google Scholar 

  • Molica, R. J. R., E. J. A. Oliveira, P. V. V. C. Carvalho, A. N. S. F. Costa, M. C. C. Cunha, G. L. Melo & S. M. F. O. Azevedo, 2005. Occurrence of saxitoxins and an anatoxin-a(s)-like anticholinesterase in a Brazilian drinking water supply. Harmful Algae 4: 743–753.

    Article  CAS  Google Scholar 

  • Moreira, C., A. Fathalli, V. Vasconcelos & A. Antunes, 2015. Phylogeny and biogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Archiv für Mikrobiologie 197: 47–52.

    Article  CAS  Google Scholar 

  • Nalewajko, C. & T. P. Murphy, 2001. Effects of temperature, and availability of nitrogen and phosphorus on the abundance of Anabaena and Microcystis in Lake Biwa, Japan: an experimental approach. Limnology 2: 45–48.

    Article  Google Scholar 

  • Novak, J. T. & D. E. Brune, 1985. Inorganic carbon limited growth kinetics of some freshwater algae. Water Research 19: 215–225.

    Article  CAS  Google Scholar 

  • Padisák, J., 1997. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv für Hydrobiologie Supplementband Monographische Beiträge 107: 563–593.

    Google Scholar 

  • Paerl, H. W. & J. Huisman, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.

    Article  CAS  PubMed  Google Scholar 

  • Piccini, C., L. Aubriot, A. Fabre, V. Amaral, M. Gonza, A. Giani, C. C. Figueredo, L. Vidal, C. Kruk & S. Bonilla, 2011. Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae 10: 644–653.

    Article  Google Scholar 

  • Pierangelini, M., S. Stojkovic, P. T. Orr & J. Beardall, 2014. Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. Journal of Phycology 50: 292–302.

    Article  CAS  Google Scholar 

  • Posselt, A. J., M. A. Burford & G. Shaw, 2009. Pulses of phosphate promote dominance of the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. Journal of Phycology 45: 540–546.

    Article  CAS  Google Scholar 

  • R Core Team, 2012. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Reynolds, C. S., R. L. Oliver & A. E. Walsby, 1987. Cyanobacterial dominance: the role of buoyancy regulation in dynamic lake environments. New Zealand Journal of Marine and Freshwater Research 21: 379–390.

    Article  Google Scholar 

  • Robarts, R. D. & T. Zohary, 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.

    Article  CAS  Google Scholar 

  • Rzymski, P., B. Poniedziałek, M. Kokociński, T. Jurczak, D. Lipski & W. Wiktorowicz, 2014. Interspecific allelopathy in cyanobacteria: Cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae 35: 1–8.

    Article  CAS  Google Scholar 

  • Saker, M. L. & D. J. Griffiths, 2000. The effect of temperature on growth and cylindrospermospsin content of seven isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from water bodies in Northern Australia. Phycologia 39: 349–354.

    Article  Google Scholar 

  • Saker, M. L. & D. J. Griffiths, 2001. Occurrence of blooms of the cyanobacterium Cylindrospermopsis raciborskii (Woloszyńska) Seenayya and Subba Raju in a north Queensland domestic water supply. Marine & Freshwater Research 52: 907–915.

    Article  CAS  Google Scholar 

  • Shafik, H. M., S. Herodek, M. Présing & L. Vörös, 2001. Factors effecting growth and cell composition of cyanoprokaryote Cylindrospermopsis raciborskii (Wołoszyńska) Seenayya et Subba Raju. Archiv für Hydrobiologie Supplementband Algological Studies 140: 75–93.

    CAS  Google Scholar 

  • Shatwell, T., A. Nicklisch & J. Köhler, 2012. Temperature and photoperiod effects on phytoplankton growing under simulated mixed layer light fluctuations. Limnology and Oceanography 57: 541–553.

    Article  Google Scholar 

  • Sinha, R., L. A. Pearson, T. W. Davis, M. A. Burford, P. T. Orr & B. A. Neilan, 2012. Increased incidence of Cylindrospermopsis raciborskii in temperate zones - Is climate change responsible? Water Research 46: 1408–1419.

    Article  CAS  PubMed  Google Scholar 

  • Smith, V. H., 1983. Low nitrogen to phosphorus ratios favour dominance by blue-green algae in lake phytoplankton. Science 221: 669–671.

    Article  CAS  PubMed  Google Scholar 

  • Soares, M. C. S., M.I. de A. Rocha, M. M. Marinho, S. M. F. O. Azevedo, C. W. C. Branco & V. L. M. Huszar, 2009. Changes in species composition during annual cyanobacterial dominance in a tropical reservoir: physical factors, nutrients and grazing effects. Aquatic Microbial Ecology 57: 137–149.

  • Swan, B. K., B. Tupper, A. Sczyrba, F. M. Lauro, M. Martinez-Garcia, J. M. Gonzalez, H. Luof, J. J. Wright, Z. C. Landry, N. W. Hanson, B. P. Thompson, N. J. Poulton, P. Schwientek, S. G. Acinas, S. J. Giovannoni, M. A. Moran, S. J. Hallam, R. Cavicchioli, T. Woyke & R. Stepanauskas, 2013. Prevalent genome streamlining and latitudinal divergence of planktonic bacteria in the surface ocean. Proceedings of the National Academy of Sciences of the United States of America 110: 11463–11468.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thomas, M. K., C. T. Kremer, C. A. Klausmeier & E. Litchman, 2012. A global pattern of thermal adaptation in marine phytoplankton. Science 338: 1085–1088.

    Article  CAS  PubMed  Google Scholar 

  • Tilman, D., 1982. Resource Competition and Community Structure. Princeton University Press, Princeton, NJ.

    Google Scholar 

  • Tilman, D. & R. L. Kiesling, 1984. Freshwater algal ecology: taxonomic trade-offs in the temperature dependence of nutrient competitive abilities. In Klug, M. J. & C. A. Reddy (eds), Current Perspectives in Microbial Ecology: Proceedings of the Third International Symposium on Microbial Ecology. American Society for Microbiology, Washington, D.C.: 314–319.

    Google Scholar 

  • Uehlinger, V. U., 1981. Experimental studies of the autecology of Aphanizomenon flos-aquae. Archiv für Hydrobiologie Supplementband Algological Studies 60: 260–288.

    CAS  Google Scholar 

  • Vitousek, P. M., S. Hättenschwiler, L. Olander & S. Allison, 2002. Nitrogen and nature. Ambio 31: 97–101.

    Article  PubMed  Google Scholar 

  • Walther, G.-R., A. Roques, P. E. Hulme, M. T. Sykes, P. Pyšek, I. Kühn & M. Zobel, 2009. Alien species in a warmer world: risks and opportunities. Trends in Ecology & Evolution 24: 686–693.

    Article  Google Scholar 

  • Wiedner, C., J. Rücker, R. Brüggemann & B. Nixdorf, 2007. Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia 152: 473–484.

    Article  PubMed  Google Scholar 

  • Wilson, A. E., W. A. Wilson & M. E. Hay, 2006. Intraspecific variation in growth and morphology of the bloom-forming cyanobacterium Microcystis aeruginosa. Applied and Environmental Microbiology 72: 7386–9.  

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Acknowledgements

We thank Carole Lembi and Julianne Dyble-Bressie for providing us with C. raciborskii cultures, Alan Wilson for M. aeruginosa cultures, and G. G. Mittelbach, J. A. Lau, and C. A. Klausmeier for useful comments on the manuscript. This research was in part supported by the NSF grants (DEB 06-10531 and DEB 08-45932) to E.L., a grant by the J.S. McDonnell Foundation to C. Klausmeier and E. L. and an MSU College of Natural Science fellowship to M.K.T. This is Kellogg Biological Station Contribution No. 1711.

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  1. Mridul K. Thomas

    Present address: Department of Aquatic Ecology, Eawag: Swiss Federal Institute for Aquatic Science and Technology, Ueberlandstrasse 133, 8600, Duebendorf, Switzerland

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  1. W. K. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, 49060, USA

    Mridul K. Thomas & Elena Litchman

  2. Department of Zoology, Michigan State University, East Lansing, MI, 48824, USA

    Mridul K. Thomas & Elena Litchman

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Thomas, M.K., Litchman, E. Effects of temperature and nitrogen availability on the growth of invasive and native cyanobacteria. Hydrobiologia 763, 357–369 (2016). https://doi.org/10.1007/s10750-015-2390-2

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