Vertical Heterogeneity of Genotypic Structure and Toxic Potential within Populations of the Harmful Cyanobacterium Microcystis aeruginosa

Benjamin Misson, Delphine Latour

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Clermont Université, Université Blaise Pascal, LMGE, Clermont-Ferrand, France.

DOI: 10.4236/aim.2013.36A004                

Abstract

We investigated the vertical variability of toxic potential (i.e. proportions of cells containing microcystin genes) and genotypic structure within different populations of Microcystis aeruginosa that developed in deep artificial reservoirs on the Loire River (France). We demonstrated that a great qualitative vertical heterogeneity could exist within a single bloom of this cyanobacterium in deep lakes. Indeed, we observed important vertical shifts of both toxic potential and genotypic structure, whatever the bloom magnitude. These variations occurred mainly within the euphotic zone and proved to occur independently from abundance vertical shifts. One of the most striking results of this study is that the genotypic structure of a population of M. aeruginosa was more variable between different depths sampled at a single site than between different sites of the same reservoir sampled on top of the water column. In the same way the proportion of potentially toxic cells was sometimes more variable vertically than horizontally. The occurrence of such vertical heterogeneity in three different blooms suggests that this could be a frequent pattern within populations of M. aeruginosa.

Keywords

Cyanobacteria; Microcystis aeruginosa; Genetic Structure; Toxic Potential; Vertical Heterogeneity

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	S. M. Azevedo, W. W. Carmichael, E. M. Jochimsen, K. L. Rinehart, S. Lau, G. R. Shaw and G. K. Eaglesham, “Human Intoxication by Microcystins during Renal Dialysis Treatment in Caruaru-Brazil,” Toxicology, Vol. 181-182, 2002, pp. 441-446. http://dx.doi.org/10.1016/S0300-483X(02)00491-2
[2]	P. J. Oberholster, J. G. Myburgh, D. Govender, R. Bengis and A. M. Botha, “Identification of Toxigenic Microcystis Strains after Incidents of Wild Animal Mortalities in the Kruger National Park, South Africa,” Ecotoxicology and Environmental Safety, Vol. 72, No. 4, 2009, pp. 1177-1182. http://dx.doi.org/10.1016/j.ecoenv.2008.12.014
[3]	L. Giannuzzi, D. Sedan, R. Echenique and D. Andrinolo, “An Acute Case of Intoxication with Cyanobacteria and Cyanotoxins in Recreational Water in Salto Grande Dam, Argentina,” Marine Drugs, Vol. 9, No. 11, 2011, pp. 2164-2175. http://dx.doi.org/10.3390/md9112164
[4]	M. Sabart, D. Pobel, D. Latour, J. Robin, M.-J. Salencon and J.-F. Humbert, “Spatiotemporal Changes in the Genetic Diversity in French Bloom-Forming Populations of the Toxic Cyanobacterium Microcystis aeruginosa,” Environmental Microbiology Reports, Vol. 1, No. 4, 2009, pp. 263-272. http://dx.doi.org/10.1111/j.1758-2229.2009.00042.x
[5]	Y. Tanabe and M. M. Watanabe, “Local EXPANSION of a Panmictic Lineage of Water Bloom-Forming Cyanobacterium Microcystis aeruginosa,” PloS one, Vol. 6, No. 2, 2011, Article ID: e17085. http://dx.doi.org/10.1371/journal.pone.0017085
[6]	I. van Gremberghe, F. Leliaert, J. Mergeay, P. Vanormelingen, K. Van der Gucht, A. E. Debeer, G. Lacerot, L. De Meester and W. Vyverman, “Lack of Phylogeographic Structure in the Freshwater Cyanobacterium Microcystis aeruginosa Suggests Global Dispersal,” PloS one, Vol. 6, No. 5, 2011, Article ID: e19561. http://dx.doi.org/10.1371/journal.pone.0019561
[7]	D. Pobel, J. J. Godon, J.-F. Humbert and J. Robin, “High-Frequency Monitoring of the Genetic Diversity and the Potential Toxicity of a Microcystis aeruginosa Bloom in a French Shallow Lake,” FEMS Microbiology Ecology, Vol. 79, No. 1, 2012, pp. 132-141. http://dx.doi.org/10.1111/j.1574-6941.2011.01203.x
[8]	M. Sabart, D. Pobel, E. Briand, B. Combourieu, M.-J. Salencon, J.-F. Humbert and D. Latour, “Spatiotemporal Variations in Microcystin Concentrations and in the Proportions of Microcystin-Producing Cells in Several Microcystis aeruginosa Populations,” Applied and Environmental Microbiology, Vol. 76, No. 14, 2010, pp. 4750-4759. http://dx.doi.org/10.1128/AEM.02531-09
[9]	V. Vasconcelos, J. Morais and M. Vale, “Microcystins and Cyanobacteria Trends in a 14 Years Monitoring of a Temperate Eutrophic Reservoir (Aguieira, Portugal),” Journal of Environmental Monitoring, Vol. 13, No. 3, 2011, pp. 668-672. http://dx.doi.org/10.1039/c0em00671h
[10]	Y. Zilliges, J. C. Kehr, S. Meissner, K. Ishida, S. Mikkat, M. Hagemann, A. Kaplan, T. Borner and E. Dittmann, “The Cyanobacterial Hepatotoxin Microcystin Binds to Proteins and Increases the Fitness of Microcystis under Oxidative Stress Conditions,” PloS one, Vol. 6, No. 3, 2011, Article ID: e17615. http://dx.doi.org/10.1371/journal.pone.0017615
[11]	B. Misson, F. Donnadieu-Bernard, J. J. Godon, C. Amblard and D. Latour, “Short-and Long-Term Dynamics of the Toxic Potential and Genotypic Structure in Benthic Populations of Microcystis,” Water Research, Vol. 46, No. 5, 2012, pp. 1438-1446. http://dx.doi.org/10.1016/j.watres.2011.11.011
[12]	B. Misson, M. Sabart, C. Amblard and D. Latour, “Benthic Survival of Microcystis: Long-Term Viability and Ability to Transcribe Microcystin Genes,” Harmful Algae, Vol. 13, 2012, pp. 20-25. http://dx.doi.org/10.1016/j.hal.2011.09.010
[13]	J. M. H. Verspagen, E. Snelder, P. M. Visser, J. Huisman, L. R. Mur and B. W. Ibelings, “Recruitment of Benthic Microcystis (Cyanophyceae) to the Water Column: Internal Buoyancy Changes or Resuspension?” Journal of Phycology, Vol. 40, No. 2, 2004, pp. 260-270. http://dx.doi.org/10.1111/j.1529-8817.2004.03174.x
[14]	K. Schone, S. Jaenichen, T. Ihle, F. Ludwig and J. Benndorf, “Arriving in Better Shape: Benthic Microcystis as Inoculum for Pelagic Growth,” Harmful Algae, Vol. 9, No. 5, 2010, pp. 494-503. http://dx.doi.org/10.1016/j.hal.2010.03.005
[15]	B. Misson, M. Sabart, C. Amblard and D. Latour, “Involvement of Microcystins and Colony Size in the Benthic Recruitment of the Cyanobacterium Microcystis (Cyanophyceae),” Journal of Phycology, Vol. 47, No. 1, 2011, pp. 42-51. http://dx.doi.org/10.1111/j.1529-8817.2010.00943.x
[16]	B. Misson and D. Latour, “Influence of Light, Sediment Mixing, Temperature and Duration of the Benthic Life Phase on the Benthic Recruitment of Microcystis,” Journal of Plankton Research, Vol. 34, No. 2, 2012, pp. 113-119. http://dx.doi.org/10.1093/plankt/fbr093
[17]	M. Watanabe, K. Kaya and N. Takamura, “Fate of the Toxic Cyclic Heptapeptides, the Microcystins, from Blooms of Microcystis (Cyanobacteria) in a Hypertrophic Lake,” Journal of Phycology, Vol. 28, No. 6, 1992, pp. 761-767. http://dx.doi.org/10.1111/j.0022-3646.1992.00761.x
[18]	K. Sivonen and G. Jones, “Cyanobacterial Toxins,” In: I. Chorus and J. Bartram, Eds., Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management, E&FN Spon, London, 1999, pp. 44-111.
[19]	M. Kaebernick, B. A. Neilan, T. B0rner and E. Dittmann, “Light and the Transcriptional Response of the Microcystin Biosynthesis Gene Cluster,” Applied and Environmental Microbiology, Vol. 66, No. 8, 2011, pp. 3387-3392. http://dx.doi.org/10.1128/AEM.66.8.3387-3392.2000
[20]	M. Kaebernick and B. A. Neilan, “Ecological and Molecular Investigations of Cyanotoxin Production,” FEMS Microbiology Ecology, Vol. 35, No. 1, 2001, pp. 1-9. http://dx.doi.org/10.1111/j.1574-6941.2001.tb00782.x
[21]	E. Carrillo, L. M. Ferrero, C. Alonso-Andicoberry, A. Basanta, A. Martin, V. Lopez-Rodas and E. Costas, “Interstrain Variability in Toxin Production in Populations of the Cyanobacterium Microcystis aeruginosa from Water-Supply Reservoirs of Andalusia and Lagoons of Donana National Park (Southern Spain),” Phycologia, Vol. 42, No. 3, 2003, pp. 269-274. http://dx.doi.org/10.2216/i0031-8884-42-3-269.1
[22]	R. Kurmayer, G. Christiansen and I. Chorus, “The Abundance of Microcystin-Producing Genotypes Correlates Positively with Colony Size in Microcystis sp. and Determines Its Microcystin Net Production in Lake Wannsee,” Applied and Environmental Microbiology, Vol. 69, No. 2, 2003, pp. 787-795. http://dx.doi.org/10.1128/AEM.69.2.787-795.2003
[23]	W. E. A Kardinaal, I. Janse, M. Kamstvan Agterveld, M. Meima, J. Snoek, L. R. Mur, J. Huisman, G. Zwart and P. M. Visser, “Microcystis Genotype Succession in Relation to Microcystin Concentrations in Freshwater Lakes,” Aquatic Microbial Ecology, Vol. 48, No. 1, 2007, pp. 1-12. http://dx.doi.org/10.3354/ame048001
[24]	H. W. Paerl and J. Huisman, “Climate—Blooms Like It Hot,” Science, Vol. 320, No. 5872, 2008, pp. 57-58. http://dx.doi.org/10.1126/science.1155398
[25]	E. Briand, N. Escoffier, C. Straub, M. Sabart, C. Quiblier and J.-F. Humbert, “Spatiotemporal Changes in the genetic Diversity of a Bloom-Forming Microcystis Aeruginosa (Cyanobacteria) Population,” ISME Journal, Vol. 3, No. 4, 2009, pp. 419-429. http://dx.doi.org/10.1038/ismej.2008.121
[26]	M. Sabart, B. Misson, A. Descroix, E. Duffaud, B. Combourieu, M.-J. Salencon and D. Latour, “The Importance of Small Colonies in Sustaining Microcystis Population Exposed to Mixing Conditions: An Exploration through Colony Size, Genotypic Composition and Toxic Potential,” Environmental Microbiology Reports, 2013. http://dx.doi.org/10.1111/1758-2229.12077
[27]	C. S. Bozarth, A. D. Schwartz, J. W. Shepardson, F. S. Colwell and T. W. Dreher, “Population Turnover in a Microcystis Bloom Results in Predominantly Nontoxigenic Variants Late in the Season,” Applied and Environmental Microbiology, Vol. 76, No. 15, 2010, pp. 5207-5213. http://dx.doi.org/10.1128/AEM.00001-10
[28]	A. M. Hotto, M. F. Satchwell and G. M. Boyer, “Molecular Characterization of Potential Microcystin-Producing Cyanobacteria in Lake Ontario Embayments and Nearshore Waters,” Applied and Environmental Microbiology, Vol. 73, No. 14, 2007, pp. 4570-4578. http://dx.doi.org/10.1128/AEM.00001-10
[29]	L. Wormer, S. Cirés and A. Quesada, “Importance of Natural Sedimentation in the Fate of Microcystins,” Chemosphere, Vol. 82, No. 8, 2011, pp. 1141-1146. http://dx.doi.org/10.1016/j.chemosphere.2010.11.024
[30]	S. Rabouille and M.-J. Salencon, “Functional Analysis of Microcystis Vertical Migration: A Dynamic Model as a Prospecting Tool. II: Influence of Mixing, Thermal Stratification and Colony Diameter on Biomass Production,” Aquatic Microbiol Ecology, Vol. 39, No. 3, 2005, pp. 281-292. http://dx.doi.org/10.3354/ame039281
[31]	D. Latour, H. Giraudet and M.-J. Salencon, “Sampling Method Adapted for Colonial Cyanobacteria in a Lake Environment. Case Study of Microcystis aeruginosa in the Grangent Reservoir (Loire, France),” Comptes Rendus Biologie, Vol. 327, No. 2, 2004, pp. 105-113. http://dx.doi.org/10.1016/j.crvi.2003.12.005
[32]	C. S. Reynolds, “The Ecology of Freshwater Phytoplankton,” Cambridge University Press, Cambridge, 1984, 384 p.
[33]	D. Latour, M.-J. Salencon, J. L. Reyss and H. Giraudet, “Sedimentary Imprint of Microcystis aeruginosa (Cyanobacteria) Blooms in Grangent Reservoir (Loire, France),” Journal of Phycology, Vol. 43, No. 3, 2007, pp. 417-425. http://dx.doi.org/10.1111/j.1529-8817.2007.00343.x
[34]	C. Reynolds and G. Jaworski, “Enumeration of Natural Microcystis Populations,” British Phycological Journal, Vol. 13, No. 3, 1978, pp. 269-277. http://dx.doi.org/10.1080/00071617800650331
[35]	J.-F. Humbert and B. Le Berre, “Genetic Diversity in Two Species of Freshwater Cyanobacteria, Planktothrix (Oscillatoria) rubescens and P. agardhii,” Archive für Hydrobiology, Vol. 150, No. 2, 2001, pp. 197-206.
[36]	B. Sen, J. Hamelin, V. Bru-Adan, J. J. Godon and T. S. Chandra, “Structural Divergence of Bacterial Communities from Functionally Similar Laboratory-Scale Vermicomposts Assessed by PCR-CE-SSCP”, Journal of Applied Microbiology, Vol. 105, No. 6, 2008, pp. 2123-2132. http://dx.doi.org/10.1111/j.1365-2672.2008.03911.x
[37]	P. Loisel, B. Haegeman, J. Hamelin, J. Harmand and J. J. Godon, “A Method for Measuring the Biological Diversity of a Sample,” European Patent, 2009, Patent No. EP20553401.
[38]	M. Welker, H. Von Dohren, H. Tauscher, C. E. W. Steinberg and M. Erhard, “Toxic Microcystis in Shallow Lake Müggelsee (Germany): Dynamics, Distribution, Diversity,” Archiv für Hydrobiologie, Vol. 157, No. 2, 2003, pp. 227-248. http://dx.doi.org/10.1127/0003-9136/2003/0157-0227
[39]	T. W. Davis, D. L. Berry, G. L. Boyer and C. G. Gobler, “The Effects of Temperature and Nutrients on the Growth and Dynamics of Toxic and Non-Toxic Strains of Microcystis during Cyanobacteria Blooms,” Harmful Algae, Vol. 8, No. 5, 2009, pp. 715-725. http://dx.doi.org/10.1016/j.hal.2009.02.004
[40]	J. M. H. Verspagen, E. Snelder, P. M. Visser, K. D. Johnk, B. W. Ibelings, L. R. Mur and J. Huisman, “Benthic-Pe-lagic Coupling in the Population Dynamics of the Harmful Cyanobacterium microcystis,” Freshwater Biology, Vol. 50, No. 5, 2005, pp. 854-867. http://dx.doi.org/10.1111/j.1365-2427.2005.01368.x
[41]	R. H. Thomas and A. E. Walsby, “Buoyancy Regulation in a Strain of Microcystis,” Journal of General Microbiology, Vol. 131, No. 4, 1985, pp. 799-809. http://dx.doi.org/10.1099/00221287-131-4-799
[42]	P. M. Visser, B. W. Ibelings and L. R. Mur, “Automnal sedimentation of Microcystis spp. as Result of an Increase in Carbohydrate Ballast at Reduced Temperature,” Journal of Plankton research, Vol. 17, No. 5, 1995, pp. 919-933. http://dx.doi.org/10.1093/plankt/17.5.919
[43]	R. R. Phelan and T. G. Downing, “A Growth Advantage for Microcystin Production by Microcystis PCC7806 under High Light,” Journal of Phycology, Vol. 47, No. 6, 2011, pp. 1241-1246. http://dx.doi.org/10.1111/j.1529-8817.2011.01056.x
[44]	E. Briand, M. Bormans, C. Quiblier, M.-J. Salencon and J.-F. Humbert, “Eviden