Skip to main content
Log in

Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Cyanobacteria are the Earth’s oldest oxygenic photoautotrophs and have had major impacts on shaping its biosphere. Their long evolutionary history (∼3.5 by) has enabled them to adapt to geochemical and climatic changes, and more recently anthropogenic modifications of aquatic environments, including nutrient over-enrichment (eutrophication), water diversions, withdrawals, and salinization. Many cyanobacterial genera exhibit optimal growth rates and bloom potentials at relatively high water temperatures; hence global warming plays a key role in their expansion and persistence. Bloom-forming cyanobacterial taxa can be harmful from environmental, organismal, and human health perspectives by outcompeting beneficial phytoplankton, depleting oxygen upon bloom senescence, and producing a variety of toxic secondary metabolites (e.g., cyanotoxins). How environmental factors impact cyanotoxin production is the subject of ongoing research, but nutrient (N, P and trace metals) supply rates, light, temperature, oxidative stressors, interactions with other biota (bacteria, viruses and animal grazers), and most likely, the combined effects of these factors are all involved. Accordingly, strategies aimed at controlling and mitigating harmful blooms have focused on manipulating these dynamic factors. The applicability and feasibility of various controls and management approaches is discussed for natural waters and drinking water supplies. Strategies based on physical, chemical, and biological manipulations of specific factors show promise; however, a key underlying approach that should be considered in almost all instances is nutrient (both N and P) input reductions; which have been shown to effectively reduce cyanobacterial biomass, and therefore limit health risks and frequencies of hypoxic events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Alexova R, Fujii M, Birch D et al (2011) Iron uptake and toxin synthesis in the bloom-forming Microcystis aeruginosa under iron limitation. Environ Microbiol 13(4):1064–1077

    PubMed  CAS  Google Scholar 

  2. Ahern KS, Ahern CR, Udy JW (2007) Nutrient additions generate prolific growth of Lyngbya majuscula (cyanobacteria) in field and bioassay experiments. Harmful Algae 6:134–151

    CAS  Google Scholar 

  3. Bidle KD, Falkowski PG (2004) Cell death in planktonic, photosynthetis microorganisms. Nature Reviews Microbiol 2:643–655

    CAS  Google Scholar 

  4. Boesch DF, Burreson E, Dennison W et al (2001) Factors in the decline of coastal ecosystems. Science 293:629–638

    Google Scholar 

  5. Bormans M, Ford PW, Fabbro L (2005) Spatial and temporal variability in cyanobacterial populations controlled by physical processes. J Plankton Res 27(1):61–70

    Google Scholar 

  6. Boyer EW, Howarth RW, Galloway JN, Dentener FJ, Green PA, Vorosmarty CJ (2006) Riverine nitrogen export from the continents to the coasts. Glob Biogeochem Cycl 20. doi:10.1029/2005GB002537 GB1S91

  7. Bouvy M, Falcão D, Marinho M et al (2000) Occurence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquat Microb Ecol 23:13–27

    Google Scholar 

  8. Briand J, Leboulanger C, Humbert J et al (2004) Cylindrospermopsis raciborskii (Cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? J Phycol 40:231–238

    Google Scholar 

  9. Breitbart M, Rohwer F (2005) Here a virus, there a virus, everywhere the same virus? Trends Microbiol 13(6):278–284

    PubMed  CAS  Google Scholar 

  10. Breitbart M (2012) Marine viruses: truth or dare. Annu Rev Mar Sci 4:425–448

    Google Scholar 

  11. Burch MD, Baker PD, Steffensen DA et al (1994) Critical flow and blooms of the cyanobacterium Anabaena circinalis in the River Murray. S. Australia. Proceedings of Environmental Flows Seminar, Canberra, pp 44–51

    Google Scholar 

  12. Butterwick C, Heaney SI, Talling JF (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. J Freshwater Biol 50:291–300

    Google Scholar 

  13. Calandrino ES, Paerl HW (2011) Determining the potential for the proliferation of the harmful cyanobacterium Cylindrospermopsis raciborskii in Currituck Sound, North Carolina. Harmful Algae 11:1–9

    Google Scholar 

  14. Carmichael WW (2001) Health effects of toxin producing cyanobacteria: the cyanoHABs. Human EcolRisk Assess 7:1393–1407

    Google Scholar 

  15. Carr NG, Whitton BA (1982) The biology of cyanobacteria. Blackwell, Oxford

    Google Scholar 

  16. Chapman AD, Schelske CL (1997) Recent appearance of Cylindrospermopsis (Cyanobacteria) in five hypereutrophic Florida lakes. J Phycol 33:191–195

    Google Scholar 

  17. Chorus I, Bartram J (1999) Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management. E&F Spon, London

    Google Scholar 

  18. Chow-Fraser P, Trew DO, Findlay D et al (1994) A test of hypotheses to explain the sigmoidal relationship between total phosphorus and chlorophyll a concentrations in Canadian lakes. Can J Fish Aquat Sci 51:2052–2065

    Google Scholar 

  19. Christoffersen K, Lyck S, Winding A (2002) Microbial activity and bacterial community structure during degradation of microcystins. Aquat Microb Ecol 27:125–136

    Google Scholar 

  20. Cirés S, Wörmer L, Wiedner C et al (2012) Temperature-dependent dispersal strategies of Aphanizomenon ovalisporum (Nostocales, Cyanobacteria): implications for the annual life cycle. Microb Ecol. doi:10.1007/s00248-012-0109-8

  21. Conley DJ, Paerl HW, Howarth RW et al (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015

    PubMed  CAS  Google Scholar 

  22. Cox PA, Banack SA, Murch SJ et al (2005) Diverse taxa of cyanobacteria produce β-N-methylamino-l-alanine, a neurotoxic amino acid. Proc Natl Acad Sci USA 102(14):5074–5078

    PubMed  CAS  Google Scholar 

  23. D’Elia CF, Sanders JG, Boynton WR (1986) Nutrient enrichment studies in a coastal plain estuary: phytoplankton growth in large scale, continuous cultures. Can J Fish Aquat Sci 43:397–406

    Google Scholar 

  24. Davis TW, Berry DL, Boyer GL et al (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8(5):715–725

    CAS  Google Scholar 

  25. DeMott WR, Zhang Q-X, Carmichael WW (1991) Effects of toxic cyanobacteria and purified toxins on the survival and feeding of a copepod and three species of Daphnia. Limnol Oceanogr 36(7):1346–1357

    CAS  Google Scholar 

  26. Deng L, Hayes PK (2008) Evidence for cyanophages active against bloom-forming freshwater cyanobacteria. Freshw Biol 53(6):1240–1252

    CAS  Google Scholar 

  27. Dionisio Pires LM, Jonker RR, Van Donk E et al (2004) Selective grazing by adults and larvae of the zebra mussel (Dreissena polymorpha): application of flow cytometry to natural seston. Freshw Biol 49(1):116–126

    Google Scholar 

  28. Downing JA, Watson SB, McCauley E (2001) Predicting cyanobacteria dominance in lakes. Can J Fish Aquat Sci 58:1905–1908

    Google Scholar 

  29. Downing TG, Meyer C, Gehringer MM et al (2005) Microcystin content of Microcystis aeruginosa is modulated by nitrogen uptake rate relative to specific growth rate or carbon fixation rate. Environ Toxicol 20(3):257–262

    PubMed  CAS  Google Scholar 

  30. Dziallas C, Grossart H (2011) Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS One 6(9):25569

    Google Scholar 

  31. Edwards DJ, Marquez BL, Nogle LM et al (2004) Structure and biosynthesis of the jamaicamides, new mixed polyketide-peptide neurotoxins from the marine cyanobacterium Lyngbya majuscula. Chem Biol 11(6):817–833

    PubMed  CAS  Google Scholar 

  32. Elliott JA (2010) The seasonal sensitivity of cyanobacteria and other phytoplankton to changes in flushing rate and water temperature. Glob Change Biol 16:864–876

    Google Scholar 

  33. Elmgren R, Larsson U (2001) Nitrogen and the Baltic Sea: managing nitrogen in relation to phosphorus. The Scientific World 1(S2):371–377

    Google Scholar 

  34. Elser JJ (1999) The pathway to noxious cyanobacteria blooms in lakes: the food web as the final turn. Freshwater Biol 42:537–543

    Google Scholar 

  35. Elser JJ, Bracken MES, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1124–1134

    Google Scholar 

  36. Ferber LR, Levine SN, Lini A et al (2004) Do cyanobacteria dominate in eutrophic lakes because they fix atmospheric nitrogen? Freshw Biol 49:690–708

    CAS  Google Scholar 

  37. Ferrão-Filho AS, Azevedo SM, DeMott WR (2000) Effects of toxic and non-toxic cyanobacteria on the life history of tropical and temperate cladocerans. Freshw Biol 45:1–19

    Google Scholar 

  38. Fisher TR, Gustafson AB, Sellner K et al (1999) Spatial and temporal variation in resource limitation in Chesapeake Bay. Mar Biol 133:763–778

    Google Scholar 

  39. Fogg GE (1969) The physiology of an algal nuisance. Proc R Soc London B 173:175–189

    Google Scholar 

  40. Foy RH, Gibson CE, Smith RV (1976) The influence of daylength, light intensity and temperature on the growth rates of planktonic blue-green algae. Eur J Phycol 11:151–163

    Google Scholar 

  41. Fuhrman JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399:541–547

    PubMed  CAS  Google Scholar 

  42. Fulton RS III, Paerl HW (1987) Toxic and inhibitory effects of the blue-green alga Microcystis aeruginosa on herbivorous zooplankton. J Plankton Res 9(5):837–855

    Google Scholar 

  43. Fulton RS III, Paerl HW (1987) Effects of colonial morphology on zooplankton utilization of algal resources during blue-green algal (Microcystis aeruginosa) blooms. Limnol Oceanogr 32(3):634–644

    Google Scholar 

  44. Fulton RS III, Paerl HW (1988) Effects of the blue-green alga Microcystis aeruginosa on zooplankton competitive relations. Oecologia 76:383–389

    Google Scholar 

  45. Gallon JR (1992) Tansley review no. 44/reconciling the incompatible: N2 fixation and O2. New Phytol 122:571–609

    CAS  Google Scholar 

  46. Galloway JN, Cowling EB, Seitzinger SP et al (2002) Reactive nitrogen: too much of a good thing. Ambio 31:60–63

    PubMed  Google Scholar 

  47. Galloway JN, Cowling EB (2002) Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71

    PubMed  Google Scholar 

  48. Giani A, Bird DF, Prairie YT et al (2005) Empirical study of cyanobacterial toxicity along a trophic gradient of lakes. Can J Aquat Sci 62:2100–2109

    CAS  Google Scholar 

  49. Ginn HP, Pearson LA, Neilan BA (2010) NtcA from Microcystis aeruginosa PCC 7806 is autoregultory and binds to the microcystin promoter. Appl Environ Microbiol 76(13):4362–4368

    PubMed  CAS  Google Scholar 

  50. Gliwicz ZM (1990) Why do cladocerans fail to control algal blooms? Hydrobiologia 200–201(1):83–97

    Google Scholar 

  51. Gosselain V, VirouxL DJ-P (1998) Can a community of small-bodied grazers control phytoplankton in rivers? Freshw Biol 39:9–24

    Google Scholar 

  52. Grzebyk D, Berland B (1995) Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J Plankton Res 18:1837–1849

    Google Scholar 

  53. Haghseresht F, Wang S, Do DD (2009) A novel lanthanum-modified bentonite, Phoslock, for phosphate removal from wastewaters. Appl Clay Sci 46:369–375

    CAS  Google Scholar 

  54. Harada K, Tsuji K, Watanabe MF et al (1996) Stability of microcystins from cyanobacteria-III. Effect of pH and temperature Phycologia 25(6):83–88

    Google Scholar 

  55. Herrmann R (1996) The daily changing pattern of hydrogen peroxide in New Zealand surface waters. Environ Toxicol Chem 15(5):652–662

    CAS  Google Scholar 

  56. Hewson I, O’Neil JM, Dennison WC (2001) Virus-like particles associated with Lyngbya majuscule (Cyanophyta; Oscillatoriacea) bloom decline in Moreton Bay, Australia. Aquat Microb Ecol 25(3):207–213

    Google Scholar 

  57. Howarth RW, Marino R, Lane J et al (1988) Nitrogen fixation in freshwater, estuarine, and marine ecosystems. 2. Biogeochemical controls. Limnol Oceanogr 33(688–70):1

    Google Scholar 

  58. Huisman J, Sharples J, Stroom J et al (2004) Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85:2960–2970

    Google Scholar 

  59. Huisman JM, Matthijs HCP, Visser PM (2005) Harmful cyanobacteria. springer aquatic ecology series 3. Springer, Dordrecht, The Netherlands, 243p

    Google Scholar 

  60. Ibelings BW, Mur LR, Walsby AE (1991) Diurnal changes in buoyancy and vertical distribution in populations of Microcystis in two shallow lakes. J Plankt Res 13:419–436

    Google Scholar 

  61. Ibelings BW, Vonk M, Los HFJ et al (2003) Fuzzy modeling ofcyanobacterial surface waterblooms: validation with NOAA-AVHRR satellite images. Ecol Appl 13:1456–1472

    Google Scholar 

  62. Ishida K, Welker M, Christiansen G et al (2009) Plasticity and evolution of aeruginosin biosynthesis in cyanobacteria. Appl Environ Microbiol 75(7):2017–2026

    PubMed  CAS  Google Scholar 

  63. Jeppesen E, Søndergaard M, Meerhoff M et al (2007) Shallow lake restoration by nutrient loading reduction—some recent findings and challenges ahead. Hydrobiologia 584:239–252

    CAS  Google Scholar 

  64. Jöhnk KD, Huisman J, Sharples J et al (2008) Summer heatwaves promote blooms of harmful cyanobacteria. Glob Change Biol 14:495–512

    Google Scholar 

  65. Kaebernick M, Neilan BA, Börner T et al (2000) Light and the transcriptional response of the microcystin biosynthesis gene cluster. Appl Environ Microbiol 66(8):3387–3392

    PubMed  CAS  Google Scholar 

  66. Kahru M, Leppänen J-M, Rud O (1993) Cyanobacterial blooms cause heating of the sea surface. Marine Ecol Prog Ser 101:1–7

    Google Scholar 

  67. Kononen K, Kuparinen J, Mäkelä K et al (1996) Initiation of cyanobacyterial blooms in a frontal region at the entrance to the Gulf of Finland. Limnol Oceanogr 41:98–112

    CAS  Google Scholar 

  68. Krawiec RW (1982) Autecology and clonal variability of the marine centric diatom Thalassiosira rotula (Bacillariophyceae) in response to light, temperature, and salinity. Mar Biol 69:79–89

    Google Scholar 

  69. Kudo I, Miyamoto M, Noiri Y et al (2000) Combined effects of temperature and iron on the growth and physiology of the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J Phycol 36:1096–1102

    CAS  Google Scholar 

  70. Kurmayer R, Kutzenberger T (2003) Application of real-time PCR for quantification of microcystin genotypes in a population of the toxic cyanobacterium Microcystis sp. Appl Environ Microbiol 69:6723–6730

    PubMed  CAS  Google Scholar 

  71. Lenski RE (1988) Dynamics of interactions between bacteria and virulent bacteriophage. Adv Microb Ecol 10:1–44

    CAS  Google Scholar 

  72. Leonard JA, Paerl HW (2005) Zooplankton community structure, micro-zooplankton grazing impact, and seston energy content in the St. Johns river system, Florida as influenced by the toxic cyanobacterium Cylindrospermopsis raciborskii. Hydrobiologia 537:89–97

    Google Scholar 

  73. Lewis WM Jr, Wurtsbaugh WA (2008) Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. Inter Rev Ges Hydrobiol 93:446–465

    CAS  Google Scholar 

  74. Lewis WM Jr, Wurtsbaugh WA, Paerl HW (2011) Rationale for control of anthropogenic nitrogen and phosphorus in inland waters. Environ Sci Technol 45:10030–10035

    Google Scholar 

  75. Likens GE (ed) (1972) Nutrients and eutrophication, American Society of Limnology Oceanography special symposium 1.American Society of Limnology Oceanography

  76. Litaker RW, Warner VE, Rhyne C et al (2002) Effect of diel and interday variations in lighton the cell division pattern and in situ growthrates of the bloom-forming dinoflagellate Heterocapsa triquetra. Mar Ecol Prog Ser 232:63–74

    Google Scholar 

  77. Lyck S (2004) Simultaneous changes in cell quotas of microcystin, chlorophyll a, protein and carbohydrate during different growth phases of a batch culture experiment with Microcystis aeruginosa. J Plankton Res 26(7):727–736

    CAS  Google Scholar 

  78. Mann NH, Cook A, Millard A et al (2003) Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424:741

    PubMed  CAS  Google Scholar 

  79. Mann NH, Clokie MR, Millard A et al (2005) The genome of S-PM2, a “photosynthetic” T4-type bacteriophage that infects marine Synechococcus strains. J Bacteriol 187:3188–3200

    PubMed  CAS  Google Scholar 

  80. Mathias CB, Kirschner AKT, Velimirov B (1995) Seasonal variations of virus abundance and viral control of the bacterial production in a backwater system of the Danube River. Appl Environ Microbiol 61:3734–3740

    PubMed  CAS  Google Scholar 

  81. Mazur-Marzec H, Żeglińska L, Pliński M (2005) The effect of salinity on the growth, toxin production, and morphology of Nodularia spumigena isolated from the Gulf of Gdansk, southern Baltic Sea. J Appl Phycol 17:171–175

    CAS  Google Scholar 

  82. Miller MA, Kudela RM, Mekebri A et al (2010) Evidence for a novel marine harmful algal bloom: cyanotoxin (microcystin) transfer from land to sea otters. PLoS One 5(9):e12576

    PubMed  Google Scholar 

  83. Mitrovic SM, Oliver RL, Rees C et al (2003) Critical flow velocities for the growth and dominance of Anabaena circinalis in some turbid freshwater rivers. Freshw Biol 48:164–174

    Google Scholar 

  84. Moisander PH, McClinton E III, Paerl HW (2002) Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planktonic cyanobacteria. Microb Ecol 43:432–442

    PubMed  CAS  Google Scholar 

  85. Montangnolli W, Zamboni A, Luvizotto-Santos R et al (2004) Acute effects of Microcystis aeruginosa from the Patos Lagoon estuary, southern Brazil, on the microcrustacean Kalliapseudes schubartii (Crustacea: Tanaidacea). Arch Environ Contam Toxicol 46(4):463–469

    Google Scholar 

  86. Neilan BA, Pearson LA, Muenchhoff J et al (2012) Environmental conditions that influence toxin biosynthesis in cyanobacteria. Environ Microbiol. doi:10.1111/j.1462-2920.2012.02729.x

  87. Newell RIE (2004) Ecosystem influences of natural and cultivated populations of suspension-feeding bivalve molluscs: a review. J Shellfish Res 23(1):51–61

    Google Scholar 

  88. Nixon SW (1995) Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41:199–219

    Google Scholar 

  89. Osborne NJ, Shaw GR, Webb PM (2007) Health effects of recreational exposure to Moreton Bay, Australia waters during a Lyngbya majuscula bloom. Environ Internat 33:309–314

    CAS  Google Scholar 

  90. Otten TG, Xu H, Qin B et al (2012) Spatiotemporal patterns and ecophysiology of toxigenic Microcystis blooms in Lake Taihu, China: implications for water quality management. Environ Sci Technol 46:3480–3488

    PubMed  CAS  Google Scholar 

  91. Padisák J (1997) Cylindrospermopsis raciborskii (Woloszyńska) Seenaya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Arch Hydrobiol Suppl 107:563–593

    Google Scholar 

  92. Paerl HW, Tucker J, Bland PT (1983) Carotenoid enhancement and its role in maintaining blue-green algal (Microcystis aeruginosa) surface blooms. Limnol Oceanogr 28:847–857

    CAS  Google Scholar 

  93. Paerl HW, Bland PT, Bowles ND et al (1985) Adaptation to high intensity, low wavelength light among surface blooms of the cyanobacterium Microcystis aeruginosa. Appl Environ Microbiol 49:1046–1052

    PubMed  CAS  Google Scholar 

  94. Paerl HW (1988) Nuisance phytoplankton blooms in coastal, estuarine, and inland waters. Limnol Oceanogr 33:823–847

    CAS  Google Scholar 

  95. Paerl HW (1990) Physiological ecology and regulation of N2 fixation in natural waters. Adv Microb Ecol 11:305–344

    CAS  Google Scholar 

  96. Paerl HW (1997) Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as “new” nitrogen and other nutrient sources. Limnol Oceanogr 42:1154–1165

    CAS  Google Scholar 

  97. Paerl HW, Fulton RS III, Moisander PH et al (2001) Harmful freshwater algal blooms, with an emphasis on cyanobacteria. The Scientific World 1:76–113

    CAS  Google Scholar 

  98. Paerl HW, Fulton RS III (2006) Ecology of harmful cyanobacteria. In: Graneli E, Turner J (eds) Ecology of harmful marine algae. Springer, Berlin, pp 95–107

    Google Scholar 

  99. Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58

    PubMed  CAS  Google Scholar 

  100. Paerl HW, Joyner JJ, Joyner AR et al (2008) Co-occurrence of dinoflagellate and cyanobacterial harmful algal blooms in southwest Florida coastal waters: a case for dual nutrient (N and P) input controls. Mar Ecol Progr Ser 371:143–153

    CAS  Google Scholar 

  101. Paerl HW, Piehler MF (2008) Nitrogen and marine eutrophication. In: D.G, Capone, M. Mulholland, E. Carpenter (eds.) Nitrogen in the marine environment, vol. 2. Academic Press, Orlando, pp. 529–567

  102. Paerl HW (2009) Controlling eutrophication along the freshwater–marine continuum: dual nutrient (N and P) reductions are essential. Estuar Coasts 32:593–601

    CAS  Google Scholar 

  103. Paerl HW, Huisman J (2009) Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ Microbiol Rep 1(1):27–37

    CAS  Google Scholar 

  104. Paerl HW, Scott JT (2010) Throwing fuel on the fire: synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environ Sci Technol 44:7756–7758

    PubMed  CAS  Google Scholar 

  105. Paerl HW, Hall NS, Calandrino ES (2011) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci Tot Environ 409:739–1745

    Google Scholar 

  106. Paerl HW, Paul V (2011) Climate change: links to global expansion of harmful cyanobacteria. Water Res 46:1349–1363

    PubMed  Google Scholar 

  107. Paerl HW, Xu H, McCarthy MJ et al (2011) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res 45:1973–1983

    PubMed  CAS  Google Scholar 

  108. Paerl HW (2012) Marine Plankton. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer, Dordrecht, pp 127–153

    Google Scholar 

  109. Paul JH (1999) Microbial gene transfer: an ecological perspective. J Mol Microbiol Biotech 1:45–50

    CAS  Google Scholar 

  110. Paul VJ (2008) Global warming and cyanobacterial harmful algal blooms. In: Hudnell, H.K. (Ed.) Cyanobacterial harmful algal blooms: state of the science and research needs. Advances in Experimental Medicine and Biology 619:239–257; Springer

  111. Peeters F, Straile D, Lorke A et al (2007) Earlier onset of the spring phytoplankton bloom in lakes of the temperate zone in a warmer climate. Glob Change Biol 13:1898–1909

    Google Scholar 

  112. Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332–13334

    PubMed  CAS  Google Scholar 

  113. Potts M, Whitton BA (2000) The biology and ecology of cyanobacteria. Blackwell Scientific, Oxford

    Google Scholar 

  114. Qin B, Zhu G, Gao G et al (2010) A drinking water crisis in lake Taihu, China: linkage to climatic variability and lake management. Environ Man 45:105–112

    Google Scholar 

  115. Rabalais NN (2002) Nitrogen in aquatic ecosystems. Ambio 31:102–112

    PubMed  Google Scholar 

  116. Rantala-Ylinen A, Känä S, Wang H et al (2011) Anatoxin-a synthetase gene cluster of the cyanobacterium Anabaena sp. strain 37 and molecular methods to detect potential producers. Appl Environ Microbiol 77(20):7271–7727

    PubMed  CAS  Google Scholar 

  117. Rapala J, Erkomaa K, Kukkonen J et al (2002) Detection of microcystins with protein phosphatase inhibition assay, high-performance liquid chromatography-UV detection and enzyme-linked immunosorbent assay comparison of methods. Anal Chim Acta 466:213–231

    CAS  Google Scholar 

  118. Rashidan KK, Bird DF (2001) Rolel of predatory bacteria in the termination of a cyanobacterial bloom. Microb Ecol 41(2):97–105

    PubMed  CAS  Google Scholar 

  119. Reynolds CS (1987) Cyanobacterial water blooms. Adv Bot Res 13:67–143

    Google Scholar 

  120. Reynolds CS (2006) Ecology of phytoplankton (ecology, biodiversity and conservation). Cambridge University Press, Cambridge

    Google Scholar 

  121. Rinta-Kanto JM, Konopko EA, DeBruyn JM et al (2009) Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae 8:665–673

    CAS  Google Scholar 

  122. Robarts RD, Zohary T (1987) Temperature effects on photosynthetic capacity, respiration, and growth rates of bloom-forming cyanobacteria. NZ J Mar Freshw Res 21:391–399

    CAS  Google Scholar 

  123. Robb M, Greenop B, Goss Z et al (2003) Application of Phoslock, an innovative phosphorous binding clay, to two Western Austrailian waterways: preliminary findings. Hydrobiologia 494:237–243

    CAS  Google Scholar 

  124. Robson BJ, Hamilton DP (2003) Summer flow event induces a cyanobacterial bloom in a seasonal Western Australian estuary. Mar Freshw Res 54:139–151

    Google Scholar 

  125. Rogalus MK, Watzin MC (2008) Evaluation of sampling and screening techniques for tiered monitoring of toxic cyanobacteria in lakes. Harmful Algae 7:504–514

    CAS  Google Scholar 

  126. Scheffer M, Rinaldi S, Gragnani A et al (1997) On the dominance of filamentous cyanobacteria in shallow turbid lakes. Ecology 78:272–282

    Google Scholar 

  127. Schindler DW (1975) Whole-lake eutrophication experiments with phosphorus, nitrogen and carbon. Verh Int Ver Theor Angew Limnol 19:3221–3231

    Google Scholar 

  128. Schindler DW, Hecky RE, Findlay DL et al (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37 year whole ecosystem experiment. Proc Nat Acad Sci USA 105:11254–11258

    PubMed  CAS  Google Scholar 

  129. Schopf JW (2000) The fossil record: tracing the roots of the cyanobacterial lineage. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer Academic, Dordrecht, pp 13–35

    Google Scholar 

  130. Scott JT, McCarthy MJ (2010) Nitrogen fixation may not balance the nitrogen pool in lakes over timescales relevant to eutrophication management. Limnol Oceangr 55:1265–1270

    CAS  Google Scholar 

  131. Sellner KG, Lacouture RV, Cibik SJ et al (1991) Importance of a winter dinoflagellate-microflagellelate bloom in the Patuxent River estuary. Estuarine Coastal Shelf Sci 32:27–42

    Google Scholar 

  132. Sellner KG, Brownlee DC, Bundy MH et al (1993) Zooplankton grazing in a Potomac River cyanobacteria bloom. Estuaries 16(4):859–872

    Google Scholar 

  133. Sevilla E, Martin-Luna B, Vela L et al (2008) Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environ Microbiol 10(10):2476–2483

    PubMed  CAS  Google Scholar 

  134. Shapiro J (1990) Current beliefs regarding dominance of blue-greens: the case for the importance of CO2 and pH. Int Verein Theor Angew Limnol Verh 24:38–54

    Google Scholar 

  135. Shelford EJ, Middelboe M, Møller EF et al (2012) Virus-driven nitrogen cycling enhances phytoplankton growth. Aquatic Microbiol Ecol 66:41–46

    Google Scholar 

  136. Sigee DC, Selwyn A, Gallois P et al (2007) Patterns of cell death in freshwater colonial cyanobacteria during the late summer bloom. Phycologia 46(3):284–292

    Google Scholar 

  137. Smith VH (1983) Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221:669–671

    PubMed  CAS  Google Scholar 

  138. Søndergaard M, Jeppesen E, Jensen HS (2012) Lake restoration. In: Bengtsson L, Herschy RW, Fairbridge RW (eds) Encyclopedia of lakes and reservoir. Springer, Berlin, pp 455–458

    Google Scholar 

  139. Spivak AC, Vanni MJ, Mette EM (2010) Moving on up: can results from simple aquatic mesocosm experiments be applied across broad spatial scales? Freshw Biol 56:279–291

    Google Scholar 

  140. Sterner RW (2008) On the phosphorus limitation paradigm for lakes. Int Rev Hydrobiol 93:433–445

    CAS  Google Scholar 

  141. Steward GF, Smith DC, Azam F (1996) Abundance and production of bacteria and viruses in the Bering and Chukchi Sea. Mar Ecol Prog Ser 131:287–300

    Google Scholar 

  142. Stüken A, Rücker J, Endrulat T et al (2006) Distribution of three alien cyanobacterial species (Nostocales) in northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45:696–703

    Google Scholar 

  143. Suikkanen S, Laamanen M, Huttunen M (2007) Long-term changes in summer phytoplankton communities of the open northern Baltic Sea. Estuar Coast Shelf Sci 71:580–592

    Google Scholar 

  144. Sullivan MB, Lindell D, Lee JA et al (2006) Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLOS Biol 4:234

    Google Scholar 

  145. Suttle CA (1994) The significance of viruses to mortality in aquatic microbial communities. Microb Ecol 28:237–243

    Google Scholar 

  146. Suttle CA (2005) Viruses in the sea. Nature 437:467–469

    Google Scholar 

  147. Tillett D, Parker DL, Neilan BA (2001) Detection of toxigenicity by a probe for the microcystin synthetase a gene (mcyA) of the cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies. Appl Environ Microbiol 67:2810–2818

    PubMed  CAS  Google Scholar 

  148. Tonk L, Bosch K, Visser PM et al (2007) Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquat Microb Ecol 46:117–123

    Google Scholar 

  149. Tooming-Klunderud A, Fewer DP, Rohrlack T et al (2008) Evidence for positive selection acting on microcystin synthetase adenylation domains in three cyanobacterial genera. BMC Evol Biol 8:256

    PubMed  Google Scholar 

  150. Tsujimura S, Okubo T (2003) Development of Anabaena blooms in a small reservoir with dense sediment akinete population, with special reference to temperature and irradiance. J Plankton Res 25:1059–1067

    Google Scholar 

  151. Tucker S, Pollard P (2005) Identification of cyanophage Ma-LBP and infection of the cyanobacterium Microcystis aeruginosa from an Australian subtropical lake by the virus. Appl Environ Microbiol 71(2):629–635

    PubMed  CAS  Google Scholar 

  152. Turner JT, Tester PA (1997) Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol Oceanogr 42:1203–1214, 5 part2

    Google Scholar 

  153. Van Donk E, Lürling M, Hessen DO et al (1997) Altered cell wall morphology in nutrient-deficient phytoplankton and its impact on grazers. Limnol Oceanogr 42(2):357–364

    Google Scholar 

  154. Vanderploeg HA, Liebig JR, Carmichael WW et al (2001) Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Can J Fish Aquat Sci 58(6):1208–1221

    CAS  Google Scholar 

  155. Ventelä A-M, Wiackowski K, Moilanen M et al (2002) The effect of small zooplankton on the microbial loop and edible algae during a cyanobacterial bloom. Freshw Biol 47:1807–1819

    Google Scholar 

  156. Visser PM, Ibelings BW, Van der Veer B et al (1996) Artificial mixing prevents nuisance blooms of the cyanobacterium Microcystis in Lake Nieuwe Meer, the Netherlands. Freshw Biol 36:435–450

    Google Scholar 

  157. Vitousek PM, Howarth RW, Likens GE et al (1997) Human alteration of the global nitrogen cycle. causes and consequences. Issues Ecol 1:1–17

    Google Scholar 

  158. Von Elert E, Wolffrom T (2001) Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnol Oceanogr 46(6):1552–1558

    Google Scholar 

  159. Wagner C, Adrian R (2009) Cyanobacteria dominance: quantifying the effects of climate change. Limnol Oceanogr 54:2460–2468

    Google Scholar 

  160. Walsby AE, Hayes PK, Boje R et al (1997) The selective advantage of buoyancy provided by gas vesicles for planktonic cyanobacteria in the Baltic Sea. New Phytol 136:407–417

    Google Scholar 

  161. Walve J, Larsson U (2007) Blooms of Baltic Sea Aphanizomenon sp. (Cyanobacteria) collapse after internal phosphorus depletion. Aquat Microbiol Ecol 49:57–69

    Google Scholar 

  162. Watanabe MF, Harada K, Matsuura K et al (1989) Heptapeptide toxin production during the batch culture of two Microcystis species (Cyanobacteria). J Appl Phycol 1:161–165

    Google Scholar 

  163. Watkinson AJ, O’Neil JM, Dennison WC (2005) Ecophysiology of the marine cyanobacterium Lyngbya majuscula (Oscillatoriaceae) in Moreton Bay, Australia. Harmful Algae 4:697–715

    CAS  Google Scholar 

  164. Weyhenmeyer GA (2001) Warmer winters: are planktonic algal populations in Sweden’s largest lakes affected? Ambio 30:565–571

    PubMed  CAS  Google Scholar 

  165. Whitton BA, Potts M (2000) The ecology of cyanobacteria: their diversity in time and space. Springer, Berlin, 0792347358

    Google Scholar 

  166. Whitton BA (2012) The ecology of cyanobacteria II: their diversity in time and space. Springer, Dordrecht, the Netherands

    Google Scholar 

  167. Wiedner C, Rücker J, Brüggemann R et al (2007) Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions. Oecologia 152:473–484

    PubMed  Google Scholar 

  168. Wilhelm SW, Carberry MJ, Eldridge ML et al (2006) Marine and freshwater cyanophages in a laurentian great lake: evidence from infectivity assays and molecular analyses of g20 genes. Appl Environ Microbiol 72(7):4957–4963

    PubMed  CAS  Google Scholar 

  169. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114

    PubMed  CAS  Google Scholar 

  170. Wood SA, Dietrich DR, Cary SC et al (2012) Increasing Microcystis cell density enhances microcystin synthesis: a mesocosm study. Inland Waters 2:17–22

    Google Scholar 

  171. World Health Organization (1999) In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water: A guide to their public health consequence, monitoring and management. Spon, London

    Google Scholar 

  172. Xu H, Paerl HW, Qin B et al (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnol Oceanogr 55:420–432

    CAS  Google Scholar 

  173. Yamamoto Y, Nakahara H (2005) The formation and degradation of cyanobacterium Aphanizomenon flos-aquae blooms: the importance of pH, water temperature, and day length. Limnol 6:1–6

    CAS  Google Scholar 

  174. Yoshida M, Yoshida T, Takashima Y et al (2007) Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations correlated with nitrate concentration in a Japanese lake. FEMS Microbiol Lett 266:49–53

    PubMed  CAS  Google Scholar 

  175. Yoshida T, Nagaski K, Takashima Y et al (2008) Ma-LMM01 infecting toxic Microcystis aeruginosa illuminates diverse cyanophage genome strategies. J Bacteriol 190(5):1762–1772

    PubMed  CAS  Google Scholar 

  176. Zilliges Y, Kehr J, Meissner S et al (2011) The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PLoS One 6(3):17615

    Google Scholar 

Download references

Acknowledgments

We thank A. Joyner and N. Hall for technical assistance and J. Huisman, J. Dyble Bressie, P. Moisander, and V. Paul for contributions and helpful discussions. This work was supported by the National Science Foundation (OCE 07269989, 0812913, 0825466, and CBET 0826819, 1230543, and Dimensions of Biodiversity 1240851), U.S. EPA-STAR project R82867701, and the NOAA/EPA-ECOHAB project NA05NOS4781194, the North Carolina Sea Grant Program R/MER-47, and California Delta Stewardship Council project 2044.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hans W. Paerl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Paerl, H.W., Otten, T.G. Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls. Microb Ecol 65, 995–1010 (2013). https://doi.org/10.1007/s00248-012-0159-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0159-y

Keywords

Navigation