Hydrogen peroxide treatment promotes chlorophytes over toxic cyanobacteria in a hyper-eutrophic aquaculture pond☆
Graphical abstract
Introduction
Eutrophication of freshwater systems is a global predicament that has important ramifications for the health of aquatic food webs, animals, and people through the promotion of cyanobacterial blooms, including taxa known to produce toxic secondary metabolites such as microcystins and saxitoxins (Neilan et al., 2013; Ibelings et al., 2014). Moreover, some cyanobacteria produce taste and odor compounds, such as geosmin and 2-Methylisoborneol (MIB), that have no known negative human health consequences but impart unpleasant musty flavors and odors in drinking water and aquaculture products (Zhang et al., 2011; Olsen et al., 2016).
Undoubtedly, controlling nutrient concentrations in aquatic systems is necessary for the long-term elimination of harmful cyanobacterial blooms; however, minimizing runoff inputs and managing both sedimentation and internal loading is challenging. Nutrient control in aquaculture is especially difficult given the need to regularly feed farmed fish. Although most water resource managers understand that reducing cyanobacterial blooms should be a long-term goal, most are keen to find solutions that create quick and noticeable improvements in water quality. Consequently, multiple methods have been developed aimed at reducing phytoplankton density or inhibiting their growth, including ultrasonication (Ahn et al., 2007a; Lürling et al., 2014), modified clays (Copetti et al., 2016), and bacterial or chemical agents (Cornish et al., 2000; Marsalek et al., 2012; Iredale et al., 2012; Greenfield et al., 2014). Although these techniques can be effective, some can harm non-target organisms or lead to chemical residual accumulation in treated ecosystems while others only produce short-lived effects (Matthijs et al., 2016). These drawbacks have prevented their popularization as control methods for cyanobacterial blooms.
Hydrogen peroxide (H2O2) is a strong oxidant that is widely used for disinfection in water treatment and is on the U.S. Food and Drug Administration (FDA) approved aquaculture drugs list for aquaculture (U.S. FDA Approved Aquaculture Drugs, assessed 11 November 2017). Since H2O2 rapidly decomposes to H2O and O2 via biological, chemical, and photochemical mechanisms during oxidation, it does not leave harmful residues in the environment. Its strong oxidizing ability also promotes algal cell mortality by producing hydroxyl radicals under light exposure, which destroys proteins, lipids, and DNA (Latifi et al., 2009). More importantly, cyanobacteria are more sensitive than other phototrophs to H2O2 because of their unique cellular structure (Drábková et al., 2007). Thus, H2O2 is expected to be a selective algaecidal compound to control cyanobacterial blooms and may be a sensible alternative to controlling cyanobacterial blooms.
Prior studies have highlighted the potential of H2O2 for controlling cyanobacteria while also promoting non-toxic phytoplankton. For example, Barroin and Feuillade (1986) found the toxicity threshold of Oscillatoria (renamed to Planktothrix) under laboratory conditions to be 1.75 mg L−1 H2O2, whereas the dominant chlorophyte, Pandorina sp, was unaffected at a 10x higher H2O2 dose. Moreover, Drábková et al. (2007) also showed that cyanobacteria were negatively affected by H2O2 at concentrations 10 times less than that of green algae and diatoms, and that high light enhanced this effect across phytoplankton taxa. Lastly, Matthijs et al. (2012) performed an unreplicated experiment in a mesotrophic lake to test if H2O2 can be used to selectively suppress cyanobacteria in natural waters without affecting other organisms. In that study, Planktothrix was reduced by 99% only 3 d after the addition of 2 mg L−1 of H2O2, while eukaryotic phytoplankton and zooplankton remained largely unaffected. More recently, a field experiment confirmed that H2O2, used as sodium carbonate peroxyhydrate (a granular source of H2O2), caused a decline of phycocyanin concentrations and cell densities but did not affect chlorophyll a concentrations (Geer et al., 2017). Clearly, hydrogen peroxide has potential for controlling cyanobacteria in diverse systems.
Since freshwater algal blooms can be dominated by one or many cyanobacterial genera, including Anabaena, Aphanizomenon, Cylindrospermopsis, Microcystis, and Planktothrix, it would be useful to know if interspecific variation exists in H2O2 toxicity thresholds across important bloom-forming genera. Past efforts aimed at using H2O2 to control cyanobacterial blooms have focused on Planktothrix and Microcystis. Few studies exist documenting the effect of H2O2 on Anabaena, Aphanizomenon, and Cylindrospermopsis. Across these studies, H2O2 toxicity thresholds span several orders of magnitude from 0.33 to 60 mg L−1 (Barrington et al., 2013; Bauza et al., 2014; Wang et al., 2012).
In this study, we assessed the toxicity of H2O2 on three filamentous and one currently unicellular but originally colonial cyanobacterial genera under laboratory conditions. Based on results from the laboratory study, we conducted a replicated, field enclosure experiment in a hyper-eutrophic aquaculture pond to investigate the effect of four different H2O2 concentrations on the plankton community, which included a dense cyanobacterial bloom dominated by toxic, filamentous Planktothrix and colonial Microcystis, as well as the associated zooplankton community.
Section snippets
Laboratory experiment
The unicellular Microcystis aeruginosa (UTEX 2667) used for the laboratory experiment study was obtained from the University of Texas at Austin culture collection. Three filamentous cyanobacterial cultures, including Anabaena flos-aquae (also called Dolichospermum flos-aquae) clone R5 (AU pond R5; isolated 15 August 2010), Planktothrix agardhii clone G24 (AU pond E24; isolated 15 August 2010), and Cylindrospermopsis raciborskii clone R2 (AU pond R2; isolated 29 August 2010), were originally
Results
The four cyanobacterial genera showed large variation in their resistance to H2O2 (Fig. 1). For example, H2O2 doses of ≥0.9 mg L−1 significantly decreased the pigment concentration (Fig. 1) and Fv/Fm value in three filamentous cyanobacteria (Fig. 2; Anabaena: P < 0.001; Cylindrospermopsis: P < 0.00001; Planktothrix: P < 0.0001) after only 1 day and was maintained at low levels for each filamentous cyanobacterial taxa until day 5 (P < 0.01). In contrast, a higher H2O2 dose (≥2.7 mg L−1) was
Discussion
Hydrogen peroxide was shown to be an effective treatment against toxigenic cyanobacteria in both laboratory- and field-based experiments. In the latter experiment, high quality and harmless chlorophytes were promoted by higher H2O2 treatments (>6.7 mg L−1), which should improve trophic transfer efficiency in productive aquatic systems. The toxicity of H2O2 to phytoplankton is mainly attributed to the production of hydroxyl radicals that destroy cell membrane integrity (Mikula et al., 2012) and
Conclusions
Blooms of cyanobacteria pose serious threats to aquatic ecosystems around the world. Consequently, a variety of techniques to control cyanobacterial blooms have been developed and tested. We were interested in further testing the utility of H2O2 in a hyper-eutrophic aquaculture pond that regularly suffers from toxic cyanobacterial blooms. Using a gradient design field experiment, we found that H2O2 doses >1.3 mg L−1 where effective at significantly reducing cyanobacteria and the hepatotoxin,
Acknowledgments
This project was supported by the National Natural Science Foundation of China (grant # 31570457), the United States Department of Agriculture’s National Institute of Food and Agriculture (grant # 2017-70007-27132), and the School of Fisheries, Aquaculture, and Aquatic Sciences and the College of Agriculture at Auburn University.
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This paper has been recommended for acceptance by Sarah Harmon.