Journal of Environment Pollution and Human Health
ISSN (Print): 2334-3397 ISSN (Online): 2334-3494 Website: http://www.sciepub.com/journal/jephh Editor-in-chief: Dibyendu Banerjee
Open Access
Journal Browser
Go
Journal of Environment Pollution and Human Health. 2015, 3(3), 70-79
DOI: 10.12691/jephh-3-3-3
Open AccessArticle

From Satellite to Genes: An Integrative Approach for Timely Monitoring of Harmful Cyanobacteria in Lake Erie Beach Water

Jiyoung Lee1, 2, , Kuo-Hsin Tseng1, 3, Feng Zhang4, Cheonghoon Lee1, 5, Jason Marion1, 6, Song Liang7, 8 and C.K. Shum9, 10

1College of Public Health, Division of Environmental Health Sciences, The Ohio State University, Columbus, Ohio, USA

2Department of Food Science & Technology, The Ohio State University, Ohio, USA

3Division of Geodetic Science, School of Earth Sciences, The Ohio State University, Columbus, Ohio, USA;Now at Center for Space and Remote Sensing Research, National Central University, Taoyuan, Taiwan

4Environmental Science Graduate Program, The Ohio State University, Columbus, Ohio, USA

5Now at Graduate School of Public Health and Institute of Health and Environment, Seoul National University, Seoul, Republic of Korea

6Now at Department of Environmental Health Science, Eastern Kentucky University

7Department of Environmental and Global Health, University of Florida, Gainesville, Florida, USA

8Emerging Pathogens Institute, University of Florida, Gainesville, Florida, USA

9Division of Geodetic Science, School of Earth Sciences, The Ohio State University, Columbus, Ohio, USA

10State Key Laboratory of Geodesy and Earth's Dynamics, Institute of Geodesy & Geophysics, CAS, Wuhan, China

Pub. Date: January 08, 2016

Cite this paper:
Jiyoung Lee, Kuo-Hsin Tseng, Feng Zhang, Cheonghoon Lee, Jason Marion, Song Liang and C.K. Shum. From Satellite to Genes: An Integrative Approach for Timely Monitoring of Harmful Cyanobacteria in Lake Erie Beach Water. Journal of Environment Pollution and Human Health. 2015; 3(3):70-79. doi: 10.12691/jephh-3-3-3

Abstract

An integrated approach for quantifying cyanotoxins was investigated using satellite remote sensing with molecular and chemical tools in Lake Erie. Remotely sensed satellite-based water color measurements with Medium Resolution Imaging Spectrometer (MERIS) were compared with in situ measurements of cyanobacteria pigments, M. aeruginosa populations (total and microcystin-producing subpopulation), and microcystin (MC) concentrations. Water samples were collected from a popular Headlands Beach in Lake Erie during the summer of 2010. The quantitative anomaly of cyanobacterial blooms between the two phycocyanin (PC) measurements demonstrated a good correlation (MERIS vs. in situ, r=0.84). PC was a better harmful cyanobacteria indicator than chlorophyll-a and correlated significantly with M. aeruginosa population (P<0.05). MC was detected in 33.8% of the samples and temporal pattern demonstrated that spikes of mcyA and PC occurred prior to MC peaks. Successful analysis within the 1 km nearshore region was another remarkable finding, which may be applicable for smaller water bodies.

Keywords:
microcystin phycocyanin satellite remote sensing Microcystis aeruginosa Lake Erie

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

Figures

Figure of 4

References:

[1]  Bolsenga, S.J, Herdendorf, C.E. 1993. Lake Erie and Lake St. Clair Handbook. Wayne State University Press.
 
[2]  Edwards, M, Johns, D.G, Leterme, S.C, Svendsen, E, Richardson, A.J. 2006. Regional climate change and harmful algal blooms in the northeast Atlantic. Limnol. Oceanogr. 51(2), 820-829.
 
[3]  Harvell, C.D, Kim, K, Burkholder, J.M, Colwell, R.R, Epstein, P.R, Grimes, D.J, Hofmann, E.E, Lipp, E.K, Osterhaus, A.D, Overstreet, R.M, Porter, J.W, Smith, G.W, Vasta, G.R. 1999. Emerging marine diseases--climate links and anthropogenic factors. Science 285, 1505-1510.
 
[4]  Janus, L.L. 2010. Climate Change Impacts from a Water Supply Perspective. Impact of Climate Change on European Lakes. In The Impact of Climate Change on European Lakes. The Netherlands, Springer. pp. 469-491.
 
[5]  Peperzak, L. 2003. Climate change and harmful algal blooms in the North Sea, Acta Oecologica 24, S139-S144.
 
[6]  Zhang, F, Lee, J, Liang, S, Shum, C.K. 2015. Cyanobacteria blooms and non-alcoholic liver disease: evidence from a county level ecological study in the United States. Environ. Health. 14:41.
 
[7]  Paerl, H.W, Hall, N.S, Calandrino, E.S. 2011. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Sci. Total Environ. 409, 1739-1745.
 
[8]  Davis, T.W, Gobler, C.J, Berry, D.L, Boyer, G.L. 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.
 
[9]  Carmichael, W.W. 1997. The cyanotoxins. Adv. Bot. Res. 27, 211-256.
 
[10]  Pelaez, M, Antoniou, M.G, He, X, Dionysiou, D.D, de la Cruz, A.A, Tsimeli, K, Triantis, T, Hiskia, A, Kaloudis, T, Williams, C, Aubel, M, Chapman, A, Foss, A, Khan, U, O'Shea, K.E, Westrick, J. 2010. Sources and occurrence of cyanotoxins worldwide. In: Fatta-Kassinos D, Bester K, Kümmerer K, editors, Xenobiotics in the Urban Water Cycle. New York, Springer. pp. 101-127.
 
[11]  Steffen, M.M, Belislea, B.S, Watsonb, S.B, Boyerc, G.L, W, W.S. 2014. Status, causes and controls of cyanobacterial blooms in Lake Erie. J. Great Lakes Res. 40, 215-225.
 
[12]  Trumpickas, J, Shuter, B.J, Minns, C.K. 2009. Forecasting impacts of climate change on Great Lakes surface water temperatures. J. Great Lakes Res. 35, 454-463.
 
[13]  Boyer, G.L. 2008. Cyanobacterial toxins in New York and the lower Great Lakes ecosystems. Adv. Exp. Med. Biol. 619, 153-165.
 
[14]  Ouellette, A.J.A, Handy, S.M, Wilhelm, S.W. 2006. Toxic Microcystis is widespread in Lake Erie: PCR detection of toxin genes and molecular characterization of associated cyanobacterial communities. Microb. Ecol. 51, 154-165.
 
[15]  Michalak, A.M, Anderson, E.J, Beletsky, D, Boland, S, Bosch, N.S, Bridgeman, T.B, Chaffin, J.D, Cho, K, Confesor, R, Daloglu, I, Depinto, J.V, Evans, M.A, Fahnenstiel, G.L, He, L, Ho, J.C, Jenkins, L, Johengen, T.H, Kuo, K.C, Laporte, E, Liu, X, McWilliams, M.R, Moore, M.R, Posselt, D.J, Richards, R.P, Scavia, D, Steiner, A.L, Verhamme, E, Wright, D.M, Zagorski, M.A. 2013. Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proc. Natl. Acad. Sci. U. S. A. 110, 6448-6452.
 
[16]  Li, C.-M, Chu, R.Y.-Y, Hsientang Hsieh, D.P. 2006. An enhanced LC-MS/MS method for microcystin-LR in lake water. J. Mass Spectrom. 41, 169-174.
 
[17]  Ahn, C.-Y, Joung, S.-H, Yoon, S.-K, Oh, H.-M. 2007. Alternative alert system for cyanobacterial bloom, using phycocyanin as a level determinant. J. Microbiol. 45(2), 98-104.
 
[18]  Marion, J.W, Lee, J, Wilkins, J.R, Lemeshow, S, Lee, C, Waletzko, E.J, Buckley, T.J. 2012. In vivo phycocyanin flourometry as a potential rapid screening tool for predicting elevated microcystin concentrations at eutrophic lakes. Environ. Sci. Technol. 46, 4523-4531.
 
[19]  McQuaid, N, Zamyadi, A, Prévost, M, Bird, D.F, Dorner, S. 2011. Use of in vivo phycocyanin fluorescence to monitor potential microcystin-producing cyanobacterial biovolume in a drinking water source. J. Environ. Monitor. 13, 455-463.
 
[20]  Li, L.H, Li, L, Shi, K, Li, Z.C, Song, K.S. 2012a. A semi-analytical algorithm for remote estimation of phycocyanin in inland waters. Sci. Total Environ. 435, 141-150.
 
[21]  Vincent, R.K, Qin, X, McKay, R.M.L, Miner, J, Czajkowski, K, Savino, J, Bridgeman, T. 2004. Phycocyanin detection from LANDSAT TM data for mapping cyanobacterial blooms in Lake Erie. Remote Sens. Environ. 89, 381-392.
 
[22]  Stumpf, R.P. 2012. Applications of satellite ocean color sensors for monitoring and predicting harmful algal blooms. Human Ecol. Risk Assessment:An Int. J. 7(5), 1363-1368.
 
[23]  Sridhar, B.B.M, Vincent, R.K. 2007. Spectral Reflectance Measurements of a Microcystis Bloom in Upper Klamath Lake, Oregon. J. Great Lakes Res. 33, 279-284.
 
[24]  Dominguez-Gómez, J.A, Alonso, C.A, Gracía, A.A. 2011. Remote sensing as a tool for monitoring water quality parameters for Mediterranean Lakes of European Union water framework directive and as a system of surveillance of cyanobacterial harmful algae blooms. Environ. Monit. Assess. 181, 317-334.
 
[25]  Guanter, L, Ruiz-Verdu, A, Odermatt, D, Giardino, C, Simis, S, Estelles, V, Heege, T, Dominguez-Gómez, J.A, Moreno, J. 2010. Atmospheric correction of ENVISAT/MERIS data over inland waters: Validation for European lakes. Remote Sens. Environ. 114, 467-480.
 
[26]  Hunter, P.D, Tyler, A.N, Gilvear, D.J, Willby, N.J. 2009. Using remote sensing to aid the assessment of human health risks from blooms of potentially toxic cyanobacteria. Environ. Sci. Technol. 43(7), 2627-2633.
 
[27]  Li, D, Kong, F, Shi, X, Ye, L, Yu, Y, Yang, Z. 2012b. Quantification of microcystin-producing and non-microcystin producing Microcystis populations during the 2009 and 2010 blooms in Lake Taihu using quantitative real-time PCR. J. Environ. Sci. 24, 284-290.
 
[28]  Agha, R, Cires, S, Wormer, L, Dominguez, J.A, Quesada, A. 2012. Multi-scale strategies for the monitoring of freshwater cyanobacteria: Reducing the sources of uncertainty. Water Res. 46(9), 3043-3053.
 
[29]  Ha, J.H, 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.
 
[30]  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 Microbiol. Lett. 266(1), 49-53.
 
[31]  Briand, E, Gugger, M, François, J.-C, Bernard, C, Humbert, J.-F, 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.
 
[32]  Lee, C, Marion, J.W, Cheung, M, Lee, C.S, Lee, J. 2015. Associations among Human-Associated Fecal Contamination, Microcystis aeruginosa, and Microcystin at Lake Erie Beaches. Int. J. Environ. Res. Public Health. 12:11466-11485.
 
[33]  Kasai, F, Kawachi, M, Erata, M, Watanabe, M.M, NIES-Collection. 2004. List of Strains, Microalgae and Protozoa, 7th edition. Tsukuba, Japan, National Institute for Environmental Studies.
 
[34]  Tillett, D, Neilan, B.A. 2000. Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J. Phycol. 36, 251-258.
 
[35]  Kutser, T. 2009. Passive optical remote sensing of cyanobacteria and other intense phytoplankton blooms in coastal and inland waters. Int. J. Remote Sens. 30, 4401-4425.
 
[36]  Ruiz-Verdú, A, Simis, S.G.H, de Hoyos, C, Gons, H.J, Peña-Martínez, R. 2008. An evaluation of algorithms for the remote sensing of cyanobacterial biomass, pp. 3996-4008.
 
[37]  Dekker, A.G. 1993. Detection of optical water quality parameters for entrophic waters by high resolution remote sensing. PhD Thesis. Free University, Amsterdam.
 
[38]  Arino, O, Gross, D, Ranera, F, Bourg, L, Leroy, M, Bicheron, P, Latham, J, Gregorio, A.D, Brockman, C, Witt, R, Defourny, P, Vancutsem, C, Herold, M, Sambale, J, Achard, F, Durieux, L, Plummer, S, Weber, J.L. 2007. GlobCover: ESA service for global land cover from MERIS. 2007 IEEE International Geoscience and Remote Sensing Symposium, pp. 2412-2415.
 
[39]  Schalles, J.F, Yacobi, Y.Z. 2000. Remote detection and seasonal patterns of phycocyanin, carotenoid, and chlorophyll pigments in eutrophic waters. Archives fur Hydrobiologia - Special Issues Advancements in Limnology. 55: 153-168.
 
[40]  Simis, S.G.H, Peters, S.W.M, Gons, H.J. 2005. Remote sensing of the cyanobacterial pigment phycocyanin in turbid inland water. Limnol. Oceanogr. 50, 237-245.
 
[41]  Randolph, K, Wilson, J, Tedesco, L, Li, L, Pascual, D.L, Soyeux, E. 2008. Hyperspectral remote sensing of cyanobacteria in turbid productive water using optically active pigments, chlorophyll a and phycocyanin. Remote Sens. Environ. 112, 4009-4019.
 
[42]  Pope, R.M, Fry, E.S. 1997. Absorption spectrum (380-700 nm) of pure water. II. Integrating cavity measurements. Appl. Opt. 36, 8710-8723.
 
[43]  Simis, S.G.H, Ruiz-Verdú, A, Domínguez-Gómez, J.A, Peña-Martinez, R, Peters, S.W.M, Gons, H.J. 2007. Influence of phytoplankton pigment composition on remote sensing of cyanobacterial biomass. Remote Sens. Environ. 106, 414-427.
 
[44]  Chawira, M. 2012. Monitoring blue-green algae in the IJsselmeer using remote sensing and in-situ measurements. MA thesis, University of Twente, Enschede, The Netherlands.
 
[45]  Giardino, C, Bresciani, M, Villa, P, Martinelli, A. 2010. Application of remote sensing in water resource management: the case study of Lake Trasimeno, Italy. Water Resour Manag. 24(14), 3885-3899.
 
[46]  Santer, R, Zagolski, F. 2009. Improve contrast between ocean and land. ATBD–MERIS level-1C, Rev. 1, Rep. D6 (1). University of Littoral, France.
 
[47]  Kratzer, S, Vinterhav, C. 2010. Improvement of MERIS level 2 products in Baltic Sea coastal areas by applying the Improved Contrast between Ocean and Land processor (ICOL) - data analysis and validation. Oceanologia 52, 211-236.
 
[48]  Binding, C.E, Greenberg, T.A, Jerome, J.H, Bukata, R.P, Letourneau, G. 2010. An assessment of MERIS algal products during an intense bloom in Lake of the Woods. J. Plankton Res. 33(5), 793-806.
 
[49]  Chapra, S.C, Dobson, H.F.H. 1981. Quantification of the Lake Trophic Typologies of Naumann (Surface Quality) and Thienemann (Oxygen) with Special Reference to the Great Lakes. International Association Great Lakes Research 7(2): 182-193.
 
[50]  World Health Organization.1998. Guidelines for drinking water quality, 2nd ed. Addendum to vol. 2. Health criteria and other supporting information. World Health Organization, Geneva, Switzerland.
 
[51]  Oliver, R.L, Ganf, G.G. 2000. In: Whitton, B.A., Potts, M. (Eds.), Freshwater Blooms. The Ecology of Cyanobacteria, Their Diversity in Time and Space. Kluwer Academic, Dordrecht, The Netherlands, pp. 149-194.
 
[52]  Long, B.M, Jones, G.J, Orr, P.T. 2001. Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Appl. Environ. Microbiol. 67, 278-283.
 
[53]  Wiedner, C, Visser, P.M, Fastner, J, Metcalf, J.S, Codd, G.A, Mur, L.R. 2003. Effects of light on the microcystin content of Microcystis strain PCC 7806. Appl. Environ. Microbiol. 69, 1475-1481.
 
[54]  Joung, S.-H, Ko, S.-R, Oh, H.-M, Ahn, C.-Y. 2011. Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae 10, 188-193.
 
[55]  Rinta-Kanto, J.M, Konopko, E.A, DeBruyn, J.M, Bourbonniere, R.A, Boyer, G.L, 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.
 
[56]  U.S. Environmental Protection Agency. 2002. Method 1603: Escherichia coli (E. coli) in water by membrane filtration using modified membrane-Thermotolerant Escherichia coli agar (modified mTEC). EPA-821-R-02-023. Office of Water, U.S. Environmental Protection Agency. Washington, D.C., USA.
 
[57]  Schalles, J.F, Yacobi. Y, Z. 2000. Remote detection and seasonal patterns of phycocyanin, carotenoid, and chlorophyll pigments in eutrophic waters. Archives fur Hydrobiologia - Special Issues Advancements in Limnology, 55: 153-168.
 
[58]  Ficek, D, Kaczmarek, S, Ston-Egiert, J, Wozniak, B, Majchrowski, R, Dera, J. 2004. Spectra of light absorption by phytoplankton pigments in the Baltic; conclusions to be drawn from a Gaussian analysis of empirical data. Oceanologia, 46(4), 533-555.
 
[59]  Chorus, I. 2005. Current approaches to cyanotoxin risk assessment, risk management and regulations in different countries. Umweltbundesamt, Dessau.