Evaluation of Size Structure in Freshwater Cyanobacterial Populations: Methods to Quantify Risk Associated with Changes in Biomass and Microcystin Concentrations — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Evaluation of Size Structure in Freshwater Cyanobacterial Populations: Methods to Quantify Risk Associated with Changes in Biomass and Microcystin Concentrations
Lim-Tex, North Andover, MA, USA
,
Department of Zoology, University of New Hampshire, Durham, NH, USA
,
Manchester Water Works, Manchester, NH, USA
,
Town of Barnstable, Barnstable, MA, USA
,
Association to Preserve Cape Cod, Dennis, MA, USA
1 Lim-Tex, North Andover, MA, USA
2 Department of Zoology, University of New Hampshire, Durham, NH, USA
3 Manchester Water Works, Manchester, NH, USA
4 Town of Barnstable, Barnstable, MA, USA
5 Association to Preserve Cape Cod, Dennis, MA, USA
Cyanobacterial populations in surface waters, including drinking water supplies and recreational waters, represent an ever present challenge for resource managers. As communities continuously respond to external and internal processes, dynamic profiles of composition, dominance, growth and toxigenicity emerge. In this study measures of size structure and biomass, quantified using light microscopy and fluorometry, were used to estimate microcystin concentrations through linear regression analysis. Toxigenic profiles using cyanobacterial biomass were developed for lakes dominated by Microcystis spp. and Dolichospermum spp., influenced by both genus-specific pigment concentrations as well as microcystin concentrations. Community composition (Log %MIC) and biomass were used to describe microcystin concentrations in mixed assemblages, where composition was the first input variable. The accessory photopigment phycocyanin was used to describe the linear relationship between the daily growth and net microcystin production rates in the bloom-forming Microcystis spp. samples, suggesting that this size-fractionated sample may provide indications of potential toxigenicity in the whole lake water sample. Future investigations using fluorometric evaluation of cyanobacterial populations could provide additional applications and metrics for use by resource managers to quantify risk association with elevated cyanotoxin concentrations.
U.S. Environmental Protection Agency (2018) 2018 Edition of the Drinking Water Standards and Health Advisory Tables. EPA 822-F-18-001.
U.S. Environmental Protection Agency (2019) Recommended Human Health Recreational Ambient Water Quality Criteria or Swimming Advisories for Microcystins and Cylindrospermopsin. EPA 822-R-19-001.
Zamyadi, A., Choo, F., Newcombe, G., Stuetz, R. and Henderson, R.K. (2016) A Review of Monitoring Technologies for Real-Time Management of Cyanobacteria: Recent Advances and Future Direction. Trends in Analytical Chemistry, 85, 83-96. https://doi.org/10.1016/j.trac.2016.06.023
Stumpf, R.P., Davis, T.W., Wynne, T.T., Graham, J.L., Loftin, K.A., Johengen, T.H., Gossiaux, D., Palladino, D. and Burtner, A. (2016) Challenges for Mapping Cyanotoxin Patterns from Remote Sensing of Cyanobacteria. Harmful Algae, 54, 160-173. https://doi.org/10.1016/j.hal.2016.01.005
Francy, D.S., Brady, A.M.G., Ecker, C.D., Graham, J.L., Stelzer, E.A., Struffolino, P., Dwyer, D.F. and Loftin, K.A. (2016) Estimating Microcystin Levels at Recreational Sites in Western Lake Erie and Ohio. Harmful Algae, 58, 23-34. https://doi.org/10.1016/j.hal.2016.07.003
Recknagel, F., Orr, P.T., Bartkow, M., Swanepoel, A. and Cao, H. (2017) Early Warning of Limit-Exceeding Concentrations of Cyanobacteria and Cyanotoxins in Drinking Water Reservoirs by Inferential Modeling. Harmful Algae, 69, 18-27. https://doi.org/10.1016/j.hal.2017.09.003
Rinta-Kanto, J.M., Konopka, 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. https://doi.org/10.1016/j.hal.2008.12.004
Newcombe, G., House, J., Ho, L., Baker, P. and Burch, M. (2010) Management Strategies for Cyanobacteria (Blue-Green Algae): A Guide for Water Utilities. Research Report 74, Water Quality Research Australia, Adelaide.
Leland, N.J. and Haney, J.F. (2018) Alternative Methods for Analysis of Cyanobacterial Populations in Drinking Water Supplies: Fluorometric and Toxicological Applications Using Phycocyanin. Journal of Water Resource and Protection, 10, 740-761. https://doi.org/10.4236/jwarp.2018.108042
U.S. Environmental Protection Agency (2010) Standard Operating Procedure for Phytoplankton Analysis. LG401, Revision 05, February 2010.
Bennett, A. and Bogorad, L. (1973) Complimentary Chromatic Adaptation in a Filamentous Blue-Green Alga. The Journal of Cell Biology, 58, 419. https://doi.org/10.1083/jcb.58.2.419
Systat Software SigmaPlot 14.
Kurmayer, R., Christiansen, G. and Chorus, I. (2003) 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, 69, 787-795. https://doi.org/10.1128/AEM.69.2.787-795.2003
Ozawa, K., Fujioka, H., Muranaka, M., Yokoyama, A., Katagami, Y., Homma, T., Ishikawa, K., Tsulimura, 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. Environmental Toxicology, 20, 270-276.
Ozawa, K., et al. (2005) Species Composition and Microcystin Concentration in Lake Biwa. Environmental Toxicology, 20, 270-276. https://doi.org/10.1002/tox.20117
Znachor, P., Jurczak, T., Komarkova, J., Jezberova, J., Mankiewicz, J., Kastovska, K. and Zapomelova, E. (2006) Summer Changes in Cyanobacterial Bloom Composition and Microcystin Concentration in Eutrophic Czech Reservoirs. Environmental Toxicology, 21, 236-243. https://doi.org/10.1002/tox.20176
Rapala, J., Sivonen, K., Lyra, C. and Niemela, S.I. (1997) Variation of Microcystins, Cyanobacterial Hepatotoxins, in Anabaena spp. as a Function of Growth Stimuli. Applied and Environmental Microbiology, 65, 2206-2212.
Pip, E. and Bowman, L. (2014) Microcystin and Algal Chlorophyll in Relation to Nearshore Nutrient Concentrations in Lake Winnipeg, Canada. Environment and Pollution, 3, 36-47. https://doi.org/10.5539/ep.v3n2p36
Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M. and Stanier, R.Y. (1979) Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria. Journal of General Microbiology, 111, 1-61. https://doi.org/10.1099/00221287-111-1-1
Bryant, D.A. (1982) Phycoerythrocyanin and Phycoerythirn: Properties and Occurrence in Cyanobacteria. Journal of General Microbiology, 128, 835-844. https://doi.org/10.1099/00221287-128-4-835
Huisman, J., Jonker, R.R., Zonneveld, C. and Weissing, F.J. (1999) Competition for Light between Phytoplankton Species: Experimental Tests of Mechanistic Theory. Ecology, 80, 211-222. https://doi.org/10.1890/0012-9658(1999)080[0211:CFLBPS]2.0.CO;2
Tandeau de Marsac, N. (1977) Occurrence and Nature of Chromatic Adaptation in Cyanobacteria. Journal of Bacteriology, 130, 82-91.
Bryant, D.A. and Cohen-Bazire, G. (1981) Effects of Chromatic Illumination on Cyanobacterial Phycobilisomes. European Journal of Biochemistry, 119, 415-424. https://doi.org/10.1111/j.1432-1033.1981.tb05624.x
Oelmuller, R., Conley, P.B., Federspiel, N., Briggs, W.R. and Grossman, A.R. (1988) Changes in Accumulation and Synthesis of Transcripts Encoding Phycobilisome Components during Acclimation of Fremyella diplosiphon to Different Light Qualities. Plant Physiology, 88, 1077-1083. https://doi.org/10.1104/pp.88.4.1077
Shih, P.M., Wu, D., Latifi, A., Axen, S.D., Fewer, D.P., Talla, E., Calteau, A., Cai, F., Tandeau de Marsac, N., Rippka, R., Herdman, M., Sivonen, K., Coursin, T., Laurent, T., Goodwin, L., Nolan, M., Davenport, K.W., Han, C.S., Rubin, E.M., Eisen, J.A., Woyke, T., Gugger, M. and Kerfeld, C.A. (2013) Improving the Coverage of the Cyanobacterial Phylum Using Diversity-Driven Genome Sequencing. Proceedings of the National Academy of Sciences, 110, 1053-1058. https://doi.org/10.1073/pnas.1217107110
Tanabe, Y. and Yamaguchi, H. (2018) Evolutionary History of Phycoerythrin Pigmentation in the Water Bloom-Forming Cyanobacterium Microcystis aeruginosa. https://doi.org/10.1101/485508
Hirose, Y., Chihong, S., Watanabe, M., Yonekawa, C., Murata, K., Ikeuchi, M. and Eki, T. (2019) Diverse Chromatic Acclimation Regulating Phycoerythrocyanin and Rod-Shaped Phycobilisome in Cyanobacteria. Molecular Plant, 12, 715-725. https://doi.org/10.1016/j.molp.2019.02.010
Chang, D.-W., Hobson, P., Burch, M. and Lin, T.-F. (2012) Measurement of Cyanobacteria Using In-Vivo Fluoroscopy-Effect of Cyanobacterial Species, Pigments and Colonies. Water Research, 46, 5037-5048. https://doi.org/10.1016/j.watres.2012.06.050
Macario, I.E., Castro, B., Nunes, M.S., Antunes, S., Pizarro, C., Coelho, C. and Goncalves, F. (2015) New Insights towards the Establishment of Phycocyanin Concentration Thresholds Considering Species-Specific Variability of Bloom-Forming Cyanobacteria. Hydrobiologia, 757, 155-165. https://doi.org/10.1007/s10750-015-2248-7
Orr, P.T. and Jones, G.J. (1998) Relationship between Microcystin Production and Cell Division Rates in Nitrogen-Limited Microcystis aeruginosa Cultures. Limnology and Oceanography, 43, 1604-1614. https://doi.org/10.4319/lo.1998.43.7.1604
Long, B.M., Jones, G.J. and Orr, P.T. (2001) Cellular Microcystin Content in N-Limited Microcystis aeruginosa Can Be Predicted from Growth Rate. Applied and Environmental Microbiology, 67, 278-283. https://doi.org/10.1128/AEM.67.1.278-283.2001
Briand, E., Bormans, M., Quiblier, C., Salencon, M.-J. and Humbert, J.-F. (2012) Evidence of the Cost of the Production of Microcystins by Microcystis aeruginosa under Differing Light and Nitrate Environmental Conditions. PLoS ONE, 7, e29981. https://doi.org/10.1371/journal.pone.0029981
Jahnichen, S., Ihle, T. and Petzoldt, T. (2008) Variability of Microcystin Cell Quota: A Small Model Explains Dynamics and Equilibria. Limnologica, 38, 339-349. https://doi.org/10.1016/j.limno.2008.05.003
Ceballos-Laita, L., Marcuello, C., Lostao, A., Calvo-Begueria, L., Velazquez-Campoy, A., Bes, M.T., Fillat, M.F. and Peleato, M.-L. (2017) Microcystin-LR Binds Iron, and Iron Promotes Self-Assembly. Environmental Science and Technology, 51, 4841-4850. https://doi.org/10.1021/acs.est.6b05939
Jahnichen, S., Petzoldt, T. and Benndorf, J. (2001) Evidence for Control of Microcystin Dynamics in Bautzen Reservoir (Germany) by Cyanobacterial Population Growth Rates and Dissolved Inorganic Carbon. Archives of Hydrobiology, 150, 177-196. https://doi.org/10.1127/archiv-hydrobiol/150/2001/177
Kardinaal, W.E.A., Tonk, L., Janse, I., Hol, S., Slot, P., Huisman, J. and Visser, P.M. (2007) Competition for Light between Toxic and Nontoxic Strains of the Harmful Cyanobacterium Microcystis. Applied and Environmental Microbiology, 73, 2939-2946. https://doi.org/10.1128/AEM.02892-06
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. https://doi.org/10.1016/j.hal.2009.02.004
Lyck, S. and Christoffersen, K. (2003) Microcystin Quota, Cell Division and Microcystin Net Production of Precultured Microcystis aeruginosa CYA 228 (Chroococcales, Cyanophyceae) under Field Conditions. Phycologia, 42, 667-674. https://doi.org/10.2216/i0031-8884-42-6-667.1
Chan, F., Pace, M.L., Howarth, R.W. and Marino, R.M. (2004) Bloom Formation in Heterocystic Nitrogen-Fixing Cyanobacteria: The Dependence on Colony Size and Zooplankton Grazing. Limnology and Oceanography, 49, 2171-2178. https://doi.org/10.4319/lo.2004.49.6.2171