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Pdf (Accessed Mankiewicz-Boczek, 2012) Ecotoxicology and Environmental Safety 114 (2015) 318–325 Contents lists available at ScienceDirect Ecotoxicology and Environmental Safety journal homepage: www.elsevier.com/locate/ecoenv Environmental influence on cyanobacteria abundance and microcystin toxin production in a shallow temperate lake Tammy A. Lee n, Gretchen Rollwagen-Bollens, Stephen M. Bollens, Joshua J. Faber-Hammond 1 School of the Environment, Washington State University, 14204 NE Salmon Creek Avenue, Vancouver, WA 98686, USA article info abstract Article history: The increasing frequency of harmful cyanobacterial blooms in freshwater systems is a commonly Received 7 May 2014 recognized problem due to detrimental effects on water quality. Vancouver Lake, a shallow, tidally Accepted 8 May 2014 influenced lake in the flood plain of the Columbia River within the city of Vancouver, WA, USA, Available online 22 July 2014 has experienced numerous summertime cyanobacterial blooms, dominated by Aphanizomenon sp. and Keywords: Anabaena sp. Cyanobacteria abundance and toxin (microcystin) levels have been monitored in this qPCR popular urban lake for several years; however, no previous studies have identified which cyanobacteria Cyanobacteria species produce toxins, nor analyzed how changes in environmental variables contribute to the ELISA fluctuations in toxic cyanobacteria populations. We used a suite of molecular techniques to analyze NMDS water samples from Vancouver Lake over two summer bloom cycles (2009 and 2010). Both intracellular MIC 16S and extracellular microcystin concentrations were measured using an ELISA kit. Intracellular microcystin mcyE concentrations exceeded WHO guidelines for recreational waters several times throughout the sampling period. PCR results demonstrated that Microcystis sp. was the sole microcystin-producing cyanobacteria species present in Vancouver Lake, although Microcystis sp. was rarely detected in microscopical counts. qPCR results indicated that the majority of the Microcystis sp. population contained the toxin-producing gene (mcyE), although Microcystis sp. abundance rarely exceeded 1 percent of overall cyanobacteria abundance. Non-metric multidimensional scaling (NMDS) revealed that PO4–P was the main environ- mental variable influencing the abundance of toxic and non-toxic cyanobacteria, as well as intracellular microcystin concentrations. Our study underscores the importance of using molecular genetic techni- ques, in addition to traditional microscopy, to assess the importance of less conspicuous species in the dynamics of harmful algal blooms. & 2014 Elsevier Inc. All rights reserved. 1. Introduction affected areas, reduced local fisheries, and increased water treatment costs (Hoagland et al., 2002; Paerl, 2008). Harmful cyanobacterial blooms are an increasingly common In addition to their broader ecological impacts, cyanobacteria occurrence in eutrophied aquatic systems, and may result in a broad are known to produce a suite of secondary metabolites that range of environmental, social, and economic consequences. For include hepatotoxins, neurotoxins, and dermatotoxic compounds. example, cyanobacterial blooms can increase oxygen demand, which These toxins have been linked to decreased water quality may lead to localized incidents of hypoxic or anoxic conditions that and detrimental effects on higher trophic levels (Leonard and lead to fish kills (Anderson et al., 2002; Paerl, 2008). Surface blooms Paerl, 2005; Ferrão-Filho et al., 2009), as well as small animal can also block light from reaching benthic primary producers, which mortality and illness (Boyer, 2007; Jacoby and Kann, 2007), and may then adversely affect food web dynamics dependent on lake- adverse health risks to humans (Paerl, 2008). A complex suite of bottom habitat (Bricelj and Lonsdale, 1997; Gallegos and Bergstrom, interacting environmental factors influence cyanobacterial bloom 2005). Social and economic impacts of cyanobacterial blooms include dynamics and toxin production. These include abiotic factors such negative effects on recreational opportunities due to closure of as nutrient inputs (Downing et al., 2001; Elliott, 2012; Heisler et al., 2008), hydrodynamics (i.e. wind-driven currents, turbulence, and stratification) (Fortin et al., 2010; Hotto et al., 2007), light availability (Cires et al., 2011; Renaud et al., 2011), and tempera- n Corresponding author. ture (Cires et al., 2011; Davis et al., 2009), but also biotic interac- E-mail address: [email protected] (T.A. Lee). 1 Current Address: Department of Biology, Portland State University, PO Box tions such as competition and grazing (Elser, 1999; Ger et al., 2010; 751, Portland, OR 97207, USA. Gobler et al., 2007). http://dx.doi.org/10.1016/j.ecoenv.2014.05.004 0147-6513/& 2014 Elsevier Inc. All rights reserved. T.A. Lee et al. / Ecotoxicology and Environmental Safety 114 (2015) 318–325 319 Not all cyanobacteria species produce toxins, therefore being able to identify and quantify the abundance of toxin and non- toxin-producing cyanobacteria is essential to understanding toxic cyanobacterial bloom dynamics. In particular, toxin and non-toxin producing individuals of the same species often coexist (Davis et al., 2009; Otsuka et al., 1999; Rantala et al., 2006), and toxin producing individuals cannot be morphologically distinguished from non-toxin producing individuals (Dittmann et al., 1997). Moreover, cyanotoxins are not species specific: several different species are known to produce the same toxin and the regulation of toxin production varies considerably as environmental conditions change. Without identifying the toxin-producing species, mana- ging for toxic cyanobacterial bloom effects on water resources may be ineffective. Vancouver Lake is a large, temperate, shallow, non-stratifying lake located in the floodplain of the Columbia River, within the city limits of Vancouver, Washington, USA. Vancouver Lake is a local recreational destination serving residents throughout the Portland (OR)-Vancouver (WA) Metropolitan area. It also serves as critical habitat for wildlife and migratory waterfowl. Cyanobacterial blooms have been documented in Vancouver Lake since 1979, although anecdotal references suggest blooms also occurred prior to that (Bhagat and Orsborn, 1971). In recent years the lake has often been closed during late summer due to cyanobacterial blooms and the presence of toxins. Although the overall plankton community of Vancouver Lake has been studied and documented (Boyer et al., 2011; Rollwagen-Bollens et al., 2012), no studies have investigated the identity of the microcystin-producing cyanobac- teria and the potential water quality variables associated with toxin production. More broadly, we are interested in Vancouver Lake as a model system to elucidate cyanobacterial bloom dynamics in shallow, temperate lakes generally. Thus the objectives of this study were Fig. 1. Vancouver Lake, Washington, is located just north of Portland, Oregon. The to use molecular genetic techniques to identify any microcystin- filled circle represents the sampling station at Vancouver Lake Sailing Club. producing species in Vancouver Lake, and to investigate which fl the phytoplankton community generally and the cyanobacteria community speci- environmental variables in uence changes in microcystin concen- fically. Samples were analyzed by the Marine Chemistry Lab at the University of tration and the toxin-producing cyanobacteria population. Washington's School of Oceanography. 2.3. Microscopic analysis 2. Materials and methods Lugol's preserved phytoplankton samples were concentrated in settling cham- 2.1. Field collection bers (r10 mL) and at least 200 cells were enumerated using an Olympus CK-40 inverted microscope (400 Â ) and identified at least to genus, and to species Sampling for the current study was conducted from the Vancouver Lake Sailing whenever possible (Prescott et al., 1978; Wehr, 2002). Club dock (Fig. 1) on a weekly basis during the periods of May through October 2009, and June through September 2010. A prior study examining the spatial 2.4. DNA extraction and purification distribution of plankton communities in Vancouver Lake showed no significant differences in plankton abundance or taxonomic composition among eight study sites throughout the lake (Bollens and Rollwagen-Bollens, 2009). Briefly, eight For DNA extraction, 250 mL aliquots of lake water were filtered onto 0.45 mm different sampling sites representing both littoral and limnetic zones were sampled GF/F filters at the time of collection. Filters were kept frozen in polyethylene on a quarterly basis for one year to measure spatial and temporal variability in centrifuge tubes at À80 1C until analyzed. Filters were initially suspended in Buffer plankton. Although there were significant seasonal differences, there were no ATL (Qiagen, Valencia, CA) and disrupted by three cycles of freezing at À20 1C and significant spatial differences among sites (Kendall's tau, p40.5), thus we consider thawing at 70 1C. Proteinase K was added to a final concentration of 50 mg/mL and the dock site to be representative of the lake as a whole. On each sampling date, incubated at 50 1C for 2 h. DNA was extracted by first adding phenol/chloroform/ vertical profiles of temperature, dissolved O2, pH, and turbidity were measured isoamyl alcohol (25:24:1) (v/v), and then a second chloroform/isoamyl alcohol every 0.2 m from the surface to the bottom using a YSI 91 probe. Total water (24:1) extraction (v/v). DNA was precipitated overnight at À20 1C after adding column
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