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Role of Environmental Factors and Toxic Genotypes in the Regulation of Microcystins-Producing Cyanobacterial Blooms

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Abstract

The aim of this study was to understand: (1) how environmental conditions can contribute to formation of Microcystis-dominated blooms in lowland, dam reservoirs in temperate climate—with the use of quantitative molecular monitoring, and (2) what is the role of toxic Microcystis genotypes in the bloom functioning. Monitoring of the Sulejow Reservoir in 2009 and 2010 in two sites Tresta (TR) and Bronislawow BR), which have different morphometry, showed that physicochemical conditions were always favorable for cyanobacterial bloom formation. In 2009, the average biomass of cyanobacteria reached 13 mg L−1 (TR) and 8 mg L−1 (BR), and in the second year, it decreased to approximately 1 mg L−1 (TR and BR). In turns, the mean number of toxic Microcystis genotypes in the total Microcystis reached 1 % in 2009, both in TR and BR, and in 2010, the number increased to 70 % in TR and 14 % in BR. Despite significant differences in the biomass of cyanobacteria in 2009 and 2010, the mean microcystins (MCs) concentration and toxicity stayed at a similar level of approximately 1 μg L−1. Statistical analysis indicated that water retention time was a factor that provided a significant difference between the two monitoring seasons and was considered a driver of the changes occurring in the Sulejow Reservoir. Hydrologic differences, which occurred between two studied years due to heavy flooding in Poland in 2010, influenced the decrease in number of Microcystis biomass by causing water disturbances and by lowering water temperature. Statistical analysis showed that Microcystis aeruginosa biomass and 16S rRNA gene copy number representing Microcystis genotypes in both years of monitoring could be predicted on the basis of total and dissolved phosphorus concentrations and water temperature. In present study, the number of mcyA gene copies representing toxic Microcystis genotypes could be predicted based on the biomass of M. aeruginosa. Moreover, MCs toxicity and concentration could be predicted on the basic of mcyA gene copy number and M. aeruginosa (biomass, 16S rRNA), respectively. Present findings may indicate that Microcystis can regulate the number of toxic genotypes, and in this way adjust the whole bloom to be able to produce MCs at the level which is necessary for its maintenance in the Sulejow Reservoir under stressful hydrological conditions.

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References

  1. Heisler J, Glibert P, Burkholder J, Anderson D, Cochlan W, Dennison W, Dortch Q, Gobler C, Heil C, Humphries E (2008) Eutrophication and harmful algal blooms: a scientific consensus. Harmful Algae 8:3–13

    Article  CAS  Google Scholar 

  2. O'Neil JM, Davis TW, Burford MA, Gobler CJ (2012) The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14:313–334

    Article  Google Scholar 

  3. Zalewski M (2000) Ecohydrology—the scientific background to use ecosystem properties as management tools toward sustainability of water resources. Ecol Eng 16:1–8

    Article  Google Scholar 

  4. Zalewski M, Robarts R (2003) Ecohydrology—a new paradigm for integrated water resources management. SIL News September 40:1–5

  5. Zalewski M (2009) Ecohydrology: a framework for reversing the degradation of the Baltic Sea. BALTEX Newsletter October 7–10

  6. Chorus I (2005) Current approaches to cyanotoxin risk assessment, risk management and regulations in different countries. WaBoLU-Hefte, Federal Environmental Agency (Umweltbundesamt) Berlin, Germany, pp. 1–9

  7. Davis TW, Berry DL, Boyer GL, Gobler CJ (2009) The effects of temperature and nutrients on the growth and dynamics of toxic and nontoxic strains of Microcystis during cyanobacterial blooms. Harmful Algae 8:715–725

    Article  CAS  Google Scholar 

  8. Dittmann E, Wiegand C (2006) Cyanobacterial toxins—occurrence biosynthesis and impact on human affairs. Mol Nutr Food Res 50(1):7–17

    Article  CAS  PubMed  Google Scholar 

  9. Doblin MA, Coyne KJ, Rinta-Kanto JM, Wilhelm SW, Dobbs FC (2007) Dynamics and short-term survival of toxic cyanobacteria species in ballast water from NOBOB vessels transiting the Great Lakes—implications for HAB invasions. Harmful Algae 6(4):519–530

    Article  CAS  Google Scholar 

  10. Dz.U. 222 (2002) Rozporządzenie ministra środowiska z dnia 23 grudnia 2002 r. w sprawie kryteriów wyznaczania wód wrażliwych na zanieczyszczenie związkami azotu ze źródeł rolniczych [Ministry of Environment Regulation; December 23rd 2002: on the criteria for designation of water bodies sensitive to pollution from nitrogen compounds from agricultural sources]

  11. El-Shehawy R, Gorokhova E, Fernández-Piñas F, Del Campo FF (2012) Global warming and hepatotoxin production by cyanobacteria: what can we learn from experiments? Water Res 46(5):1420–1429

    Article  CAS  PubMed  Google Scholar 

  12. Gan N, Xiao Y, Zhu L, Wu Z, Liu J, Hu C, Song L (2012) The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environ Microbiol 14(3):730–742

    Article  CAS  PubMed  Google Scholar 

  13. Gągała I, Izydorczyk K, Skowron A, Kamecka-Plaskota D, Stefaniak K, Kokociński M, Mankiewicz-Boczek J (2010) Appearance of toxigenic cyanobacteria in two Polish lakes dominated by Microcystis aeruginosa and Planktothrix agardhii and environmental factors influence. Ecohydrol Hydrobiol 10(1):25–34

    Article  Google Scholar 

  14. Giovannoni SJ, DeLong EF, Schmidt TM, Pace NR (1990) Tangential flow filtration and preliminary phylogenetic analysis of marine picoplankton. Appl Environ Microbiol 56(8):2572–2575

    PubMed Central  CAS  PubMed  Google Scholar 

  15. Golterman HL, Clymo RS, Ohstand MA (1978) Methods for physical and chemical analysis of freshwater. 2nd edn. Blackwell Science Inc., Oxford, 214

  16. Ha JH, Hidaka T, Tsuno H (2009) Quantification of toxic Microcystis and evaluation of its dominance ratio in blooms using real-time PCR. Environ Sci Technol 43(3):812–818

    Article  CAS  PubMed  Google Scholar 

  17. Hesse K, Dittmann E, Börner T (2001) Consequence of impaired microcystin production for light-dependent growth and pigmentation of Microcystis aeruginosa PCC 7806 FEMS. Microb Ecol 37:39–43

    Article  CAS  Google Scholar 

  18. Horn W (1991) The influence of biomass and structure of the crustacean plankton on the water transparency in the Saidenbach storage reservoir. Hydrobiologia 225:115–120

    Article  Google Scholar 

  19. Hotto AM, Satchwell MF, Berry DL, Gobler CJ, Boyer GL (2008) Spatial and temporal diversity of microcystins and microcystin-producing genotypes in Oneida Lake NY. Harmful Algae 7(5):671–681

    Article  CAS  Google Scholar 

  20. Huisman J, Matthijs HCP, Visser PM (2005) Harmful cyanobacteria. Springer aquatic ecology Series 3. Springer, Dordrecht, p 243

    Google Scholar 

  21. Izydorczyk K, Jurczak T, Wojtal-Frankiewicz A, Skowron A, Mankiewicz-Boczek J, Tarczyńska M (2008) Influence of abiotic and biotic factors on microcystin content in Microcystis aeruginosa cells in an eutrophic temperate reservoir. J Plankton Res 30(4):393–400

    Article  CAS  Google Scholar 

  22. Jang M-H, Ha K, Joo G-J, Takamura N (2003) Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwat Biol 48:1540–1550

    Article  Google Scholar 

  23. Jähnichen S, Ihle T, Petzoldt T, Benndorf J (2007) Impact of inorganic carbon availability on microcystin production by Microcystis aeruginosa PCC 7806. Appl Environ Microbiol 73:6994–7002

    Article  PubMed Central  PubMed  Google Scholar 

  24. Joung SH, Oh HM, Ko SR, Ahn CY (2011) Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae 10(2):188–193

    Article  Google Scholar 

  25. Jurczak T, Tarczyńska M, Karlsson K, Meriluoto J (2004) Characterization and diversity of cyanobacterial hepatotoxins (microcystins) in blooms from Polish freshwaters identified by liquid chromatography-electrospray ionisation mass spectrometry. Chromatographia 59(9–10):571–578

    CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Kardinaal WEA, Visser PM (2005) Dynamics of cyanobacterial toxins: sources of variability in microcystin concentrations. In: Huisman J, Matthijs HCP, Visser PM (eds) Harmful cyanobacteria. Springer, Berlin, pp 41–63

    Google Scholar 

  28. Kardinaal WEA, Janse I, Kamst-Van Agterveld M, Meima M, Snoek J, Mur LR, Huisman J, Zwart G, Visser PM (2007) Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat Microb Ecol 48:1–12

    Article  Google Scholar 

  29. Kardinaal WEA, Tonk L, Janse I, Hol S, Slot P, Huisman J, Visser PM (2007) Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis. Appl Environ Microbiol 73:2939–2946

    Article  PubMed Central  PubMed  Google Scholar 

  30. Kehr JC, Zilliges Y, Springer A, Disney MD, Ratner DD, Bouchier C, Seeberger PH, De Marsac NT, Dittmann E (2006) A mannan binding lectin is involved in cell-cell attachment in a toxic strain of Microcystis aeruginosa. Mol Microbiol 59:893–906

    Article  CAS  PubMed  Google Scholar 

  31. Kondracki J (2000) Atlas hydrologiczny Polski [Hydrological atlas of Poland]. Wyd Geol Warszawa

  32. Kurmayer R, Dittmann E, Fastner J, Chorus I (2002) Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in Lake Wannsee (Berlin Germany). Microb Ecol 43:107–118

    Article  CAS  PubMed  Google Scholar 

  33. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Lawton LA, Robertson PKJ (1999) Physico-chemical treatment methods for the removal of microcystins (cyanobacterial hepatotoxins) from potable waters. Chem Soc Rev 28:217–224

    Article  CAS  Google Scholar 

  35. LeBlanc RS, Pick FR, Fortin N (2011) Effect of light intensity on the relative dominance of toxigenic and nontoxigenic strains of Microcystis aeruginosa. Appl Environ Microbiol 77(19):7016–7022

    Article  Google Scholar 

  36. Mankiewicz J, Tarczyńska M, Jurczak T, Wojtysiak-Staniaszczyk M, Zalewski M (2003) Test with luminescent bacteria for the toxicity assessment of cyanobacterial bloom samples. FEB 12(8):861–864

    CAS  Google Scholar 

  37. Mankiewicz-Boczek J, Urbaniak M, Romanowska-Duda Z, Izydorczyk K (2006) Toxic Cyanobacteria strains in lowland dam reservoir (Sulejow Res Central Poland): amplification of mcy genes for detection and identification. Pol J Ecol 53(2):1–11

    Google Scholar 

  38. Martins A, Moreira C, Vale M, Freitas M, Regueiras A, Antunes A, Vasconcelos V (2011) Seasonal dynamics of Microcystis spp. and their toxigenicity as assessed by qPCR in a temperate reservoir. Mar Drugs 9(10):1715–1730

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Meriluoto J, Codd GA (2005) Toxic cyanobacterial monitoring and cyanotoxin analysis. Åbo Akademi University Press, Finland, p 150

    Google Scholar 

  40. Neilan BA, Jacobs D, Del Dot T, Blackall LL, Hawkins PR, Cox PT, Goodman AE (1997) rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus. Microcystis Int J Syst Bacteriol 47(3):693–697

    Article  CAS  PubMed  Google Scholar 

  41. Otten TG, Xu H, Qin B, Zhu G, Paerl HW (2012) Spatiotemporal patterns and ecophysiology of toxigenic Microcystis blooms in Lake Taihu China: implications for water quality management. Environ Sci Technol 46(6):3480–3488

    Article  CAS  PubMed  Google Scholar 

  42. Paerl H (2008) Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. Adv Exp Med Biol 619:217–237

    Article  CAS  PubMed  Google Scholar 

  43. Pearson LA, Neilan BA (2008) The molecular genetics of cyanobacterial toxicity as a basis for monitoring water quality and public health risk. Curr Opin Biotech 19:281–288

    Article  CAS  PubMed  Google Scholar 

  44. Rinta-Kanto JM, Ouellette AJA, Boyer GL, Twiss MR, Bridgeman TB, Wilhelm SW (2005) Quantification of toxic Microcystis spp. during the 2003 and 2004 blooms in western Lake Erie using quantitative real-time PCR. Sci Technol 39:4198–4205

    Article  CAS  Google Scholar 

  45. Rinta-Kanto JM, Saxton MA, DeBruyn JM, Smith JL, Marvin CH, Krieger KA, Sayler GS, Boyer GL, Wilhelm SW (2009) The diversity and distribution of toxigenic Microcystis spp. in present day and archived pelagic and sediment samples from Lake Erie. Harmful Algae 8:385–394

    Article  CAS  Google Scholar 

  46. Romo S, Soria J, Fernández F, Ouahid Y, Barón-Solá Á (2012) Water residence time and the dynamics of toxic cyanobacteria. Freshwater Biol 58(3):513–522. Doi:101111/j1365-2427201202734x

    Google Scholar 

  47. Sabart M, Pobel D, Briand E, Combourieu B, Salençon MJ, Humbert JF, Latour D (2010) Spatiotemporal variations in microcystin concentrations and in the proportions of microcystin-producing cells in several Microcystis aeruginosa populations. Appl Environ Microbiol 76(14):4750–4759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Schatz D, Keren Y, Vardi A, Sukenik A, Carmeli S, Börner T, Dittman E, Kaplan A (2007) Towards clarification of the biological role of microcystins a family of cyanobacterial toxins. Environ Microbiol 9(4):965–970

    Article  CAS  PubMed  Google Scholar 

  49. Sevilla E, Martin-Luna B, Vela L, Bes MT, Fillat MF, Peleato ML (2008) Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environ Microbiol 10:2476–2483

    Article  CAS  PubMed  Google Scholar 

  50. Sivonen K, Jones G (1999) Cyanobacterial toxins In: Chorus I, Bartram J (eds) Toxic cyanobacteria in water. A guide to their public health consequences monitoring and management. Spon Press, New York, pp. 41–111

  51. Srivastava A, Choi GG, Ahn CY, Oh HM, Ravi AK, Asthana RK (2012) Dynamics of microcystin production and quantification of potentially toxigenic Microcystis sp. using real-time PCR. Water Res 46(3):817–827

    Article  CAS  PubMed  Google Scholar 

  52. Tarczyńska M, Romanowska-Duda Z, Jurczak T, Zalewski M (2001) Toxic cyanobacterial blooms in a drinking water reservoir—causes consequences and management strategy. J Water Supply Res T 1(2):237–246

    Google Scholar 

  53. Toivola DM, Eriksson JE, Brautigan DL (1994) Identification of protein phosphatase 2A as the primary target for microcystin-LR in rat liver homogenates. FEBS Lett 344(2–3):175–180

    Article  CAS  PubMed  Google Scholar 

  54. Vaitomaa J (2006) The effects of environmental factors on biomass and microcystin production by the freshwater cyanobacterial genera Microcystis and Anabaena. Doctoral dissertation (article-based), University of Helsinki Faculty of Agriculture and Forestry Department of Applied Chemistry and Microbiology Division of Microbiology Helsinki, Finland

  55. Vaitomaa J, Rantala A, Halinen K, Rouhiainen L, Tallberg P, Mokelke L, Sivonen K (2003) Quantitative real-time PCR for determination of microcystin synthetase E copy numbers for Microcystis and Anabaena in lakes. Appl Environ Microbiol 69:7289–7297

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. van Apeldoorn ME, Van Egmond HP, Speijers GJA, Bakker GJI (2008) Toxins of cyanobacteria. Mol Nutr Food Res 51(1):7–60

    Article  Google Scholar 

  57. WHO (2011) Toxic cyanoabcteria. In: Guidelines for drinking-water quality fourth edition. Geneva, Switzerland

  58. Welker M, Šejnohová L, Némethová D, von Döhren H, Jarkovský J, Maršálek B (2007) Seasonal shifts in chemotype composition of Microcystis sp. communities in the pelagial and sediment of a shallow reservoir. Limnol Oceanogr 52:609–691

    Article  CAS  Google Scholar 

  59. Yoshida M, Yoshida T, Takashima Y, Hosoda N, Hiroishi S (2007) Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microb Lett 266:49–53

    Article  CAS  Google Scholar 

  60. Zilliges Y, Kehr JC, Mikkat S, Bouchier C, de Marsac NT, Börner T, Dittmann E (2008) An extracellular glycoprotein is implicated in cell-cell contacts in the toxic cyanobacterium Microcystis aeruginosa PCC 7806. J Bacteriol 190:2871–2879

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. Ambrożewski Z (1980) Monograph of the Sulejow reservoir. (in Polish) Warszawa WKiŁ, pp 184

  62. Wojtal A, Bogusz D, Menshutkin V, Izydorczyk K, Frankiewicz P, Zalewski M (2008) A study of Daphnia-Leptodora-juvenile Percids interactions using a mathematical model in the biomanipulated Sulejow Reservoir. Ann Limnol Int J Lim 44(1):7–23

    Article  Google Scholar 

  63. Bottrell HH, Duncan A, Gliwicz ZM, Grygierek E, Herzig A, Hilbricht-Ilkowska A, Krasawa H, Larsson P, Weglenska T (1976) A review of some problems in zooplankton production studies. Norw J Zool 24:419–456

    Google Scholar 

  64. Carmichael WW, An J (1999) Using an enzyme linked immunosorbent assay (ELISA) and protein phosphatase inhibition assay (PPIA) for the detection of microcystins and nodularins. Nat Toxins 7:377–385

    Article  CAS  PubMed  Google Scholar 

  65. Duda RO, Hart PE, Stork DG (2001) Pattern classification. Wiley, New York

    Google Scholar 

  66. Devijver PA, Kittler J (1982) Pattern recognition: a statistical approach. Prentice Hall, London

    Google Scholar 

  67. Ambrożewski Z (1993) Projektowanie i realizacja zbiornika wodnego Sulejów [Design and implementation of the water reservoir Sulejów]. Gosp Wod 12:267–273

    Google Scholar 

  68. Briand E, Gügger M, Francois JC, Bernard C, Humbert JF, Quiblier C (2008) Temporal variations in the dynamics of potentially microcystin-producing strains in a bloom-forming Planktothrix agardhii (cyanobacterium) population. Appl Environ Microbiol 74:3839–3848

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Briand E, Yéprémian C, Humbert JF, Quiblier C (2008) Competition between microcystin- and non-microcystin-producing Planktothrix agardhii (cyanobacteria) strains under different environmental conditions. Environ Microbiol 10:3337–3348

    Article  CAS  PubMed  Google Scholar 

  70. Briand E, Escoffier N, Straub C, Sabart M, Quiblier C, Humbert JF (2009) Spatiotemporal changes in the genetic diversity of a bloom-forming Microcystis aeruginosa (cyanobacteria) population. ISME J 3:419–429

    Article  CAS  PubMed  Google Scholar 

  71. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr Jussi Meriluoto from Åbo Academy (Turku, Finland) for providing the Microcystis aeruginosa strain PCC 7820. The study was financed by the National Science Centre N N305 096439. The authors would like to acknowledge the European Cooperation in Science and Technology, COST Action ES 1105 "CYANOCOST- Cyanobacterial blooms and toxins in water resources: Occurrence, impacts and management" for adding value to this study through networking and knowledge sharing with European experts and researchers in the field. The Sulejowski Reservoir is a part of the Polish National Long-Term Ecosystem Research Network and the European LTER site. It is also a monitoring and research site of the Life + EnvEurope Project LIFE08 ENV/IT/000339.

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Gągała, I., Izydorczyk, K., Jurczak, T. et al. Role of Environmental Factors and Toxic Genotypes in the Regulation of Microcystins-Producing Cyanobacterial Blooms. Microb Ecol 67, 465–479 (2014). https://doi.org/10.1007/s00248-013-0303-3

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