Effects of selenite on Microcystis aeruginosa: Growth, microcystin production and its relationship to toxicity under hypersalinity and copper sulfate stresses☆
Graphical abstract
Introduction
The Salton Sea, the largest inland lake in California, is an important habitat as a major stop-over for migratory birds traveling the Pacific Flyway (DWR, 2010). However, the Salton Sea ecosystem has been threatened by the rivers that contains remarkable concentrations of selenium (Se) (CRA, 2005), resulting from the weathering of seleniferous rocks and shales in the Upper Colorado River Basin (Presser et al., 1994) and activities of agricultural irrigation, mining and fuel burning in the Salton Basin (Schroeder et al., 2002).
Selenium is an essential micronutrient for animals with a relatively narrow margin between nutritional essentiality and potential toxicity (Young et al., 2010). High levels of Se in river and drainage water have been closely related to mortality, developmental defects, and reproductive failure in fish (Stewart et al., 2004) and waterfowl (Luoma and Presser, 2009), which was exactly the case in the Kesterson National Wildlife Refuge in California (Presser, 1994). Selenium is released into aquatic environments primarily as inorganic forms, selenite (Se (IV)) and selenate (Se (VI)), from both natural and anthropogenic sources (Morlon et al., 2006). As Se toxicity problems usually result from biomagnification in the food chain (Hartikainen, 2005), selenite is considered more toxic than selenate to aquatic wildlife (Hamilton, 2004), because the former is scavenged more easily from water and transformed to organo-selenium to a greater extent than the latter (Riedel et al., 1991). As the foundation of aquatic food chains, algae make it easier for selenite to enter the chains at the base and then quickly accumulate up along the chains (Luoma and Presser, 2009, Skorupa, 1998), increasing its bioavailability and toxicity to organisms at higher tropic levels (Fan et al., 2002, Stewart et al., 2010).
Even there has been much interest in applying freshwater algae to the bio-remediation of Se-contaminated river water due to their great ability to assimilate and volatilize Se (Huang et al., 2013, Neumann et al., 2003), the remaining Se in the algal biomass still poses the risk of Se biomagnification (Luoma and Presser, 2009). Therefore, waterborne Se in rivers that empty into the Salton Sea may have been removed from the water column by freshwater algae and accumulated in algal cells even before it reaches the Salton Sea (Neumann et al., 2003, Huang et al., 2013). In that case, freshwater algae found in rivers in the Salton Basin might play a much more important role in Se toxicity to the Salton Sea ecosystem than saltwater algae growing inside the Salton Sea. However, the fate of Se contained by these freshwater algae has never been empirically investigated after these algae are carried by rivers into the moderately hypersaline Salton Sea. In addition to hypersalinity, copper may be another stress that freshwater algae would encounter in water bodies surrounding the Salton Sea (USEPA, 2016). As one of registered or popular herbicides, copper sulfate has been used for temporary control of algae and aquatic weeds in waterways and reservoirs in southern California and Mexican border areas, including the Imperial Irrigation District located south of the Salton Sea (CalEPA, 2010).
As many studies have shown direct effects of Se on green algae, including structural damage, inhibited photosynthesis and alternations of the associated metabolism (Gojkovic et al., 2015, Riedel et al., 1996), and as trophic consequences have been considered due to the Se bioconcentration by algal species (Baines and Fisher, 2001, Baines et al., 2004), few studies have investigated Se metabolism in freshwater cyanobacteria, widely distributed over land and water, in the similar ways. Microcystis aeruginosa was selected in our study for it becomes abundant in wetlands and rivers that receive fertilizer rich irrigation water (Sivonen and Jones, 1999) and is usually blamed for eutrophication and microcystin production (Paerl et al., 2001), which is the case in the Salton Sea area. In terms of Se metabolism in microalgae, the uptake of selenate has suggested to be mediated via a sulfate transport system due to its chemical similarity to sulfur (Gojkovic et al., 2015), while there was only a little information on selenite transporter in green alga C. reinhardtii (Morlon et al., 2006) and marine calcifying microalga E. huxleyi (Araie and Shiraiwa, 2009). However, it should be noticed that the inhibition of sulfate in selenite uptake has been reported by Morlon et al. (2006), suggesting a direct competition between selenite and sulfate for transporter sites; that is, selenite may cause toxicity to M. aeruginosa through cell surface interactions (competition for transport sites) or intracellular accumulation (interference with metabolism activities). Therefore, the aim of this study was to investigate potential ecorisks to the Salton Sea ecosystem posed by freshwater algae in rivers that discharge into the lake. As selenium was supplied in the form of selenite in our experiments, M. aeruginosa was tested under different conditions, some of which could be found in the field, with the objectives to (1) determine effects of selenite on the growth and microcystin production of M. aeruginosa; (2) investigate selenite metabolism by M. aeruginosa and its potential eco-toxicity, (3) estimate impacts of sulfate on selenite assimilation and microcystin production by M. aeruginosa; and (4) determine the potential fate of selenium bearing M. aeruginosa in the Salton Sea.
Section snippets
Materials
Microcystis aeruginosa (FACHB-942) was purchased from Freshwater Algae Culture Collection at the Institute of Hydrobiology (Wuhan, China). Sodium selenite (Na2SeO3), sodium selenate (Na2SeO4), seleno-DL-methionine (SeMet; C5H11NO2Se), dl-selenocystine (C6H12N2O4Se2) and selenium standard (1000 mg/L±4 mg/L) were purchased from Sigma-Aldrich. Artificial sea salt was obtained from Blue Starfish Salt Product Co., Ltd. (Hangzhou, China), which retained the main composition of seawater. M. aeruginosa
Acute toxicity of Se on M. aeruginosa growth
The results suggest chlorophyll fluorescence parameters were affected differently as a function of selenite concentration and exposure time. Compared to control, Chla of all Se treated groups were found to be inhibited significantly (p < 0.01) over a 4-day period, which also reflected in the trend of decreasing 4 d-μ (average specific growth rate during a 4-day period) with increasing Se concentrations. Even though algae at Se concentrations of 0.1, 1 and 2 mg Se/L kept growing (p < 0.001)
Conclusion
Overall, the results of the present work show that selenite exhibited nearly indistinctive toxic effect on the growth of M. aeruginosa, with a 96 h-IC50 of 2.68 mg Se/L, which is generally higher than Se concentrations detected in natural systems except for wastewater from industrial and mining activities. However, the inhibitory effects of Se on algal growth did not lead to the decrease of microcystin production. On the contrary, selenite exposure had a positive effect on the cellular
Acknowledgements
We thank Shanghai Synchrotron Radiation Facility (SSRF) for the beam time (#15ssrf01403) granted for the Se speciation analysis. This research is funded by the Natural Science Foundation of China under grant number 51479110. We also thank the laboratory staff of the School of Environmental Science and Engineering at the Shanghai Jiao Tong University for their help with the Se analysis.
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This paper has been recommended for acceptance by Dr. Harmon Sarah Michele.