Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-23T00:31:55.510Z Has data issue: false hasContentIssue false
  • English
  • Français

Internal nutrient loading may increase microcystin concentrations in freshwater lakes by promoting growth of Microcystis populations

Published online by Cambridge University Press:  22 August 2013

Diane M. Orihel ,
Ora Hadas ,
Riki Pinkas ,
Yehudit Viner-Mozzini  and
Assaf Sukenik
Diane M. Orihel*
Affiliation:
The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, PO Box 345, Migdal 14950, Israel Present address: Department of Biological Sciences, University of Alberta, 11455 Saskatchewan Drive, Edmonton, Alberta T6G 2E9, Canada.
Ora Hadas
Affiliation:
The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, PO Box 345, Migdal 14950, Israel
Riki Pinkas
Affiliation:
The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, PO Box 345, Migdal 14950, Israel
Yehudit Viner-Mozzini
Affiliation:
The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, PO Box 345, Migdal 14950, Israel
Assaf Sukenik
Affiliation:
The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, PO Box 345, Migdal 14950, Israel
*
*Corresponding author: orihel@ualberta.ca
Get access

Abstract

Nutrient release from lake sediments may increase concentrations of harmful algal toxins – such as microcystins – by stimulating blooms of toxigenic cyanobacteria. This hypothesis is supported by a series of experiments in which intact cores of sediment were incubated under different environmental conditions, after which the water overlying the sediments was harvested as a culture medium for growing a toxic strain of the common cyanobacterium Microcystis. Both littoral and profundal sediments from Lake Kinneret, the largest freshwater lake in Israel, released substantial amounts of dissolved phosphorus (1.0 and 4.0 mg.m−2.d−1, respectively) and nitrogen (44.2 and 24.3 mg.m−2.d−1, respectively) under simulated summer conditions in the laboratory. In comparison, nutrient fluxes from sediments under simulated winter conditions were considerably smaller or negative. The addition of nutrient-rich overlying water harvested from profundal sediments, and to a lesser extent from littoral sediments, increased both chlorophyll a and microcystin concentrations in Microcystis cultures. In contrast, when Microcystis cells were inoculated in natural surface waters only, the cultures did not grow or produce microcystins, and soon collapsed. This study provides experimental evidence of a link between internal nutrient loading from sediments and microcystin concentrations in freshwaters, and demonstrates how environmental factors may indirectly exert control over toxin concentrations in freshwater lakes.

Keywords

Microcystinscyanobacterialake sedimentsinternal loadingphosphorus
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 49 , Issue 3 , 2013 , pp. 225 - 235
Copyright
© EDP Sciences, 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amé, M.V. and Wunderlin, D.A., 2005. Effects of iron, ammonium and temperature on microcystin content by a natural concentrated Microcystis aeruginosa population. Water Air Soil Pollut., 168, 235–248.CrossRefGoogle Scholar
APHA, AWWA and WEF, 2005. Standard Methods for the Examination of Water and Wastewater (21st edn,), American Public Health Association, Washington, DC.PubMed
Beresovsky, D., Hadas, O., Livne, A., Sukenik, A., Kaplan, A. and Carmeli, S., 2006. Toxins and biologically active secondary metabolites of Microcystis sp. isolated from Lake Kinneret. Isr. J. Chem., 46, 79–87.CrossRefGoogle Scholar
Bickel, H., Lyck, S. and Utkilen, H., 2000. Energy state and toxin content – experiments on Microcystis aeruginosa (Chroococcales, Cyanophyta). Phycologia, 39, 212–218.CrossRefGoogle Scholar
Briand, J.F., Jacquet, S., Bernard, C. and Humbert, J.F., 2003. Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems. Vet. Res., 34, 361–377.CrossRefGoogle ScholarPubMed
Burger, D.F., Hamilton, D.P. and Pilditch, C.A., 2008. Modelling the relative importance of internal and external nutrient loads on water column nutrient concentrations and phytoplankton biomass in a shallow polymictic lake. Ecol. Model., 211, 411–423.CrossRefGoogle Scholar
Campos, A. and Vasconcelos, V., 2010. Molecular mechanisms of microcystin toxicity in animal cells. Int. J. Mol. Sci., 11, 268–287.CrossRefGoogle ScholarPubMed
Caraco, N.F., 1993. Disturbance of the phosphorus cycle – a case of indirect effects of human activity. Trends Ecol. Evol., 8, 51–54.CrossRefGoogle ScholarPubMed
Carmichael, W.W., 1992. Cyanobacteria secondary metabolites – the cyanotoxins. J. Appl. Bacteriol., 72, 445–459.CrossRefGoogle ScholarPubMed
Carmichael, W.W., 2008. A world overview – one-hundred-twenty-seven years of research on toxic cyanobacteria – where do we go from here? In: Hudnell, H.K. (ed.), Cyanobacterial Harmful Algal Blooms, Springer, New York, 949 p.Google Scholar
Chorus, I., Falconer, I.R., Salas, H.J. and Bartram, J., 2000. Health risks caused by freshwater cyanobacteria in recreational waters. J. Toxicol. Environ. Heal. B, 3, 323–347.Google ScholarPubMed
Cymbola, J., Ogdahl, M. and Steinman, A.D., 2008. Phytoplankton response to light and internal phosphorus loading from sediment release. Freshwater Biol., 53, 2530–2542.CrossRefGoogle Scholar
Dai, R.H., Liu, H.J., Qu, J.H., Zhao, X., Ru, J. and Hou, Y.N., 2008. Relationship of energy charge and toxin content of Microcystis aeruginosa in nitrogen-limited or phosphorous-limited cultures. Toxicon, 51, 649–658.CrossRefGoogle ScholarPubMed
Davis, T.W., Berry, D.L., Boyer, G.L. and Gobler, C.J., 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, 715–725.CrossRefGoogle Scholar
Deblois, C.P. and Juneau, P., 2010. Relationship between photosynthetic processes and microcystin in Microcystis aeruginosa grown under different photon irradiances. Harmful Algae, 9, 18–24.CrossRefGoogle Scholar
Dzialowski, A.R., Wang, S.H., Lim, N.C., Beury, J.H. and Huggins, D.G., 2008. Effects of sediment resuspension on nutrient concentrations and algal biomass in reservoirs of the Central Plains. Lake Reserv. Manage., 24, 313–320.CrossRefGoogle Scholar
Ekholm, P. and Krogerus, K., 2003. Determining algal-available phosphorus of differing origin: routine phosphorus analyses versus algal assays. Hydrobiologia, 492, 29–42.CrossRefGoogle Scholar
Funari, E. and Testai, E., 2008. Human health risk assessment related to cyanotoxins exposure. Crit. Rev. Toxicol., 38, 97–125.CrossRefGoogle ScholarPubMed
Giani, A., Bird, D.F., Prairie, Y.T. and Lawrence, J.F., 2005. Empirical study of cyanobacterial toxicity along a trophic gradient of lakes. Can. J. Fish. Aquat. Sci., 62, 2100–2109.CrossRefGoogle Scholar
Grace, M.R., Scicluna, T.R., Vithana, C.L., Symes, P. and Lansdown, K.P., 2010. Biogeochemistry and cyanobacterial blooms: Investigating the relationship in a shallow, polymictic, temperate lake. Environ. Chem., 7, 443–456.CrossRefGoogle Scholar
Hadas, O., Pinkas, R., Delphine, E., Vardi, A., Kaplan, A. and Sukenik, A., 1999. Limnological and ecophysiological aspects of Aphanizomenon ovalisporum bloom in Lake Kinneret, Israel. J. Plankton Res., 21, 1439–1453.CrossRefGoogle Scholar
Head, R.M., Jones, R.I. and Bailey-Watts, A.E., 1999. Vertical movements by planktonic cyanobacteria and the translocation of phosphorus: Implications for lake restoration. Aquatic Conserv., 9, 111–120.3.0.CO;2-2>CrossRefGoogle Scholar
Holm-Hansen, O., Lorenzen, C.J., Holmes, R.W. and Strickland, J.D.H., 1965. Fluorometric determination of chlorophyll. J. Conseil, 30, 3–15.CrossRefGoogle Scholar
Jähnichen, S., Ihle, T., Petzoldt, T. and Benndorf, J., 2007. Impact of inorganic carbon availability on microcystin production by Microcystis aeruginosa PCC 7806. Appl. Environ. Microb., 73, 6994–7002.CrossRefGoogle ScholarPubMed
Jeppesen, E., Søndergaard, M., Jensen, J.P., Havens, K.E., Anneville, O., Carvalho, L., Coveney, M.F., Deneke, R., Dolulil, M.T., Foy, B., Gerdeaux, D., Hampton, S.E., Hilt, S., Kangur, K., Köhler, J., Lammens, E.H.H.R., Lauridsen, T.L., Manca, M., Miracle, M.R., Moss, B., Nõges, P., Persson, G., Phillips, G., Portielje, R., Romo, S., Schelske, C.L., Straile, D., Tatrai, I., Willén, E. and Winder, M., 2005. Lake responses to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies. Freshwater Biol., 50, 1747–1771.CrossRefGoogle Scholar
Kaplan, A., Harel, M., Kaplan-Levy, R.N., Hadas, O., Sukenik, A. and Dittmann, E., 2012. The languages spoken in the water body (or the biological role of cyanobacterial toxins). Front. Microbiol., 3, 138.CrossRefGoogle Scholar
Kardinaal, W.E.A., Janse, I., Kamst-van Agterveld, M., Meima, M., Snoek, J., Mur, L.R., Huisman, J., Zwart, G. and Visser, P.M., 2007. Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquat. Microb. Ecol., 48, 1–12.CrossRefGoogle Scholar
Kotak, B.G. and Zurawell, R.W., 2007. Cyanobacterial toxins in Canadian freshwaters: a review. Lake Reserv. Manage., 23, 109–122.CrossRefGoogle Scholar
Kotak, B.G., Lam, A.K.Y., Prepas, E.E. and Hrudey, S.E., 2000. Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Can. J. Fish. Aquat. Sci., 57, 1584–1593.CrossRefGoogle Scholar
Landsberg, J.H., 2002. The effects of harmful algal blooms on aquatic organisms. Rev. Fish. Sci., 10, 113–390.CrossRefGoogle Scholar
Lawton, L.A., Edwards, C. and Codd, G.A., 1994. Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst, 119, 1525–1530.CrossRefGoogle ScholarPubMed
Long, B.M., 2010. Evidence that sulfur metabolism plays a role in microcystin production by Microcystis aeruginosa. Harmful Algae, 9, 74–81.CrossRefGoogle Scholar
Lukač, M. and Aegerter, R., 1993. Influence of trace metals on growth and toxin production of Microcystis aeruginosa. Toxicon, 31, 293–305.CrossRefGoogle ScholarPubMed
Malmaeus, J.M. and Rydin, E., 2006. A time-dynamic phosphorus model for the profundal sediments of Lake Erken, Sweden. Aquat. Sci., 68, 16–27.CrossRefGoogle Scholar
Nalewajko, C. and Murphy, T.P., 1998. A bioassay to assess the potential effects of sediment resuspension on phytoplankton community composition. J. Appl. Phycol., 10, 341–348.CrossRefGoogle Scholar
Oh, H.M., Lee, S.J., Jang, M.H. and Yoon, B.D., 2000. Microcystin production by Microcystis aeruginosa in a phosphorus-limited chemostat. Appl. Environ. Microb., 66, 176–179.CrossRefGoogle Scholar
Orr, P.T. and Jones, G.J., 1998. Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol. Oceanogr., 43, 1604–1614.CrossRefGoogle Scholar
Ostrovsky, I., Yacobi, Y.Z., Walline, P. and Kalikhman, I., 1996. Seiche-induced mixing: its impact on lake productivity. Limnol. Oceanogr., 41, 323–332.CrossRefGoogle Scholar
Ostrovsky, I., Rimmer, A., Yacobi, Y.Z., Nishri, A., Sukenik, A., Hadas, O. and Zohary, T., 2013. Long-term changes in the Lake Kinneret ecosystem: the anthropogenic factors. In: Goldman, C.R., Kumagai, M. and Robarts, R.D. (eds.), Climate Change and Global Warming of Inland Waters: Impacts and Mitigation for Ecosystems and Societies, John Wiley and Sons, Ltd., West Sussex, 271–293.Google Scholar
Ozawa, K., Fujioka, H., Muranaka, M., Yokoyama, A., Katagami, Y., Homma, T., Ishikawa, K., Tsujimura, S., Kumagai, M., Watanabe, M.F. and Park, H.D., 2005. Spatial distribution and temporal variation of Microcystis species composition and microcystin concentration in Lake Biwa. Environ. Toxicol., 20, 270–276.CrossRefGoogle ScholarPubMed
Pearson, L., Mihali, T., Moffitt, M., Kellmann, R. and Neilan, B., 2010. On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs, 8, 1650–1680.CrossRefGoogle ScholarPubMed
Preston, T., Stewart, W.D.P. and Reynolds, C.S., 1980. Bloom-forming cyanobacterium Microcystis aeruginosa overwinters on sediment surface. Nature, 288, 365–367.CrossRefGoogle Scholar
Rantala, A., Fewer, D.P., Hisbergues, M., Rouhiainen, L., Vaitomaa, J., Börner, T. and Sivonen, K., 2004. Phylogenetic evidence for the early evolution of microcystin synthesis. P. Natl. Acad. Sci. USA, 101, 568–573.CrossRefGoogle ScholarPubMed
Rantala, A., Rajaniemi-Wacklin, P., Lyra, C., Lepistö, L., Rintala, J., Mankiewiez-Boczek, J. and Sivonen, K., 2006. Detection of microcystin-producing cyanobacteria in Finnish lakes with genus-specific microcystin synthetase gene E (mcyE) PCR and associations with environmental factors. Appl. Environ. Microb., 72, 6101–6110.CrossRefGoogle Scholar
Rinta-Kanto, J.M., Konopko, E.A., DeBruyn, J.M., Bourbonniere, R.A., Boyer, G.L. and Wilhelm, S.W., 2009. Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae, 8, 665–673.CrossRefGoogle Scholar
Serruya, C., 1978. Lake Kinneret, Dr. W. Junk Publishers, The Hague.CrossRefGoogle Scholar
Sevilla, E., Martin-Luna, B., Vela, L., Bes, M.T., Fillat, M.F. and Peleato, M.L., 2008. Iron availability affects mcyD expression and microcystin-LR synthesis in Microcystis aeruginosa PCC7806. Environ. Microbiol., 10, 2476–2483.CrossRefGoogle ScholarPubMed
Sivonen, K. and Jones, G., 1999. Cyanobacterial toxins. In: Chorus, I. and Bartram, J. (eds.), Toxic Cyanobacteria in Water – a Guide to their Public Health Consequences, Monitoring, and Management, E & FN Spon, London, 41–111.Google Scholar
Smolders, A.J.P., Lamers, L.P.M., Lucassen, E.C.H.E.T., Van Der Velde, G. and Roelofs, J.G.M., 2006. Internal eutrophication: how it works and what to do about it – a review. Chem. Ecol., 22, 93–111.CrossRefGoogle Scholar
Søndergaard, M., Jensen, J.P. and Jeppesen, E., 1999. Internal phosphorus loading in shallow Danish lakes. Hydrobiologia, 408/409, 145–152.CrossRefGoogle Scholar
Tessenow, U., Frevert, T., Hofgastner, W. and Moser, A., 1977. Ein simultan schliesender serienwasserchopfer fur sedimentkontwasser mit fotoelektrischer selbstauslosung und fakultativem sedimentstecher. Arch. Hydrobiol., 48(Supplement), 438–452.Google Scholar
Verspagen, J.M.H., Snelder, E.O.F.M., Visser, P.M., Jöhnk, K.D., Ibelings, B.W., Mur, L.R. and Huisman, J., 2005. Benthic-pelagic coupling in the population dynamics of the harmful cyanobacterium Microcystis. Freshwater Biol., 50, 854–867.CrossRefGoogle Scholar
Via-Ordorika, L., Fastner, J., Kurmayer, R., Hisbergues, M., Dittmann, E., Komarek, J., Erhard, M. and Chorus, I., 2004. Distribution of microcystin-producing and non-microcystin-producing Microcystis sp in European freshwater bodies: detection of microcystins and microcystin genes in individual colonies. Syst. Appl. Microbiol., 27, 592–602.CrossRefGoogle ScholarPubMed
Welch, E.B. and Cooke, G.D., 1995. Internal phosphorus loading in shallow lakes: importance and control. Lake Reserv. Manage., 11, 273–281.CrossRefGoogle Scholar
WHO, 2008. Guidelines for Drinking-Water Quality (3rd edn,), World Health Organization, Geneva.PubMed
Wicks, R.J. and Thiel, P.G., 1990. Environmental factors affecting the production of peptide toxins in floating scums of the cyanobacterium Microcystis aeruginosa in a hypereutrophic African reservoir. Environ. Sci. Technol., 24, 1413–1418.CrossRefGoogle Scholar
Zilliges, Y., Kehr, J.-C., Meissner, S., Ishida, K., Mikkat, S., Hagemann, M., Kaplan, A., Börner, T. and Dittmann, E., 2011. The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PloS ONE, 6, e17615.CrossRefGoogle ScholarPubMed
Zohary, T., 2004. Changes to the phytoplankton assemblage of Lake Kinneret after decades of a predictable, repetitive pattern. Freshwater Biol., 49, 1355–1371.CrossRefGoogle Scholar
Zurawell, R.W., Chen, H., Burke, J.M. and Prepas, E.E., 2005. Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. J. Toxicol. Env. Heal. B, 8, 1–37.CrossRefGoogle ScholarPubMed
Supplementary material: Image

OLM - limn 49-3(2013) Fig S1

Figure S1

Download OLM - limn 49-3(2013) Fig S1(Image)
Image 5.1 MB
Supplementary material: Image

OLM - limn 49-3(2013) Fig S2

Figure S2

Download OLM - limn 49-3(2013) Fig S2(Image)
Image 7.8 MB
Supplementary material: Image

OLM - limn 49-3(2013) Fig.S3

Figure S3

Download OLM - limn 49-3(2013) Fig.S3(Image)
Image 5.4 MB