Research PaperEffect of CO2 on growth and toxicity of Alexandrium tamarense from the East China Sea, a major producer of paralytic shellfish toxins
Introduction
Ocean acidification is a worldwide environmental problem with complex processes. Since the industrial revolution until as recently as 2011, the atmospheric partial pressure of CO2 (pCO2) has risen from 280 μatm to 430 ± 90 μatm due to the burning of fossil fuels, deforestation, industrialization, and cement production (IPCC 2014). Elevated CO2 levels will likely increase even more, with some researchers predicting levels to double up to 750–1000 μatm by the year 2100. Such elevated CO2 levels may cause ocean pH levels to decrease by as much as 0.3–0.4 units (IPCC 2014). Rising atmospheric CO2 levels is increasing seawater CO2 concentrations and is the main cause for ocean acidification. As human input of nutrients causes eutrophication, and then induce large CO2 input into coastal water (Cai et al., 2011, Sunda and Cai, 2012), the increase in atmospheric pCO2 can affect the carbon chemistry of the ocean ecosystem and may have significant implications for phytoplankton populations.
Among the many phytoplankton species that will be affected by acidification, species that cause harmful algal blooms (HABs), have received recent attention. These species, when grown outside of normal ecological levels, cause significant marine problems including mechanical damage to fish gills, toxic effects to filter-feeding invertebrates, and competition for resources (Hallegraeff, 1993, Anderson and Garrison, 1997). Recently, the frequency, scale, and distribution range of HABs are increasing worldwide (Borkman et al., 2014, van der Lingen et al., 2016, Wells et al., 2015). There are many reasons for this observation, including coastal eutrophication (Honjo, 1993, Anderson et al., 2002, Glibert et al., 2005, Hallegraeff, 2010), and major ocean biogeochemical changes such as acidification (Su et al., 2001, Cai et al., 2006, Moore et al., 2008, van der Lingen et al., 2016, Wells et al., 2015).
HAB species have the same physiological response to ocean acidification as other phytoplankton species, including altered growth and carbon fixation rates, shifts in nutrient uptake, changes in elemental ratios, and increased sensitivity to ultraviolet radiation (Riebesell, 2004, Fu et al., 2007, Fu et al., 2008a, Fu et al., 2008b, Fu et al., 2010, Fu et al., 2012, Feng et al., 2008, Feng et al., 2009, Feng et al., 2010, Hutchins et al., 2007, Hutchins et al., 2009, Riebesell et al., 2007, Riebesell et al., 2008, Rost et al., 2008, Beardall et al., 2009, Gao et al., 2012a, Gao et al., 2012b). Since ocean acidification is associated with increasing availability of dissolved inorganic carbon (DIC), increasing pCO2 concentrations are a major cause of toxic HABs. Studies have shown that under increasing pCO2 concentrations, the diatom Pseudo-nitzschia spp. demonstrated increased cellular growth rates and elevated domoic acid toxin concentrations causing amnesic shellfish poisoning (Sun et al., 2011, Tatters et al., 2012). Karlodinium veneficum, an ichthyotoxic dinoflagellate, has been shown likewise to increase growth rates and produce more carbon-based karlotoxin under elevated levels of pCO2 (Fu et al., 2010). Although the dinoflagellate Karenia brevis, which can produce brevetoxins, maintains the same toxin production per cell after rising atmospheric CO2 levels, it grows much faster and increases the likelihood of blooms. Thus, ocean acidification is expected to increase the toxicity of K. brevis blooms due to potential increases in bloom biomass yield (Errera et al., 2014, Hardison et al., 2014).
Toxic dinoflagellates within the genus Alexandrium, which cause the most widespread and dangerous HABs globally, can produce paralytic shellfish toxins (PSTs). These PSTs typically include various analogues of the following categories: (1) the carbamate compounds, including saxitoxin (STX), neosaxitoxin (NEO) and the C-11 O-sulfated gonyautoxin1–4 (GTX1, GTX2, GTX3 and GTX4); (2) N-sulfocarbamoyl analogues, which include the N- sulfocarbamoyl-II-hydroxy sulfate C toxins (C1, C2, C3 and C4), gonyautoxin 5 and 6 (GTX5 and GTX6); (3) the decarbamoyl derivates, such as decarbamoylsaxitoxin (dcSTX), decarbamoyl- neosaxitoxin (dcNEO), decarbamoylgonyautoxin 1–4 (dcGTX1, dcGTX2, dcGTX3 and dcGTX4). These compounds vary in toxic potency (Oshima, 1995) and can cause severe harm to humans consuming shellfish in polluted waters resulting in paralytic shellfish poisoning (Anderson et al., 2012). Thus, HABs of species from this genus pose a significant threat to ecological, economic, and public health issues in temperate and subarctic coastal areas worldwide (Shumway, 1990, Anderson et al., 2012). Therefore, understanding the physiological and ecological factors that control the timing and biogeography of toxic Alexandrium blooms is very important for ensuring seafood safety.
Members of the genus Alexandrium are particularly sensitive to pCO2 concentrations (Flores-Moya et al., 2012, Tatters et al., 2013, Van De Waal et al., 2014). Several toxic Alexandrium species such as A. minutum (Flores-Moya et al., 2012), A. ostenfeldii (Kremp et al., 2012), A. catenella (Fu et al., 2012, Tatters et al., 2013) and A. fundyense (Hattenrath-Lehmann et al., 2015), have shown strain specific increases in growth and toxicity when exposed to different elevated pCO2 concentrations.
A. tamarense is one of the most important species of toxic Alexandrium genus due to its global distribution. This species is also widespread in the East and South China Seas (Wang et al., 2006). A. tamarense has also been shown to have a high sensitivity to atmospheric CO2 concentrations. Van De Waal et al. (2014) investigated the impact of elevated pCO2 on PST content and composition from two strains of A. tamarense, called Alex 2 and Alex 5, isolated from the North Sea off the east coast of Scotland. These studies showed that elevated pCO2 had minor consequences for growth and toxin production in both Alex 2 and Alex 5.
In the present study, the impact of elevated pCO2 on PST production in one strain of A. tamarense, ATDH, isolated from the East China Sea was investigated. Results of these studies showed a significant response in growth and toxicity in response to elevated CO2 levels. These studies may help researchers move toward a better understanding of how this harmful bloom species may respond to the predicted future elevation of atmospheric CO2.
Section snippets
Culture conditions
A strain of A. tamarense (ATDH) was isolated from the East China Sea, and cultured to assess the effects of elevated pCO2 concentration on growth and toxicity (toxin content, toxin profiles, and cellular toxicity). Stock cultures were grown in f/2 media prepared from filtered Qingdao coastal seawater (through 0.45 μm pore size filters to remove particles) with salinity 32, enriched with phosphate, nitrogen, vitamin and trace nutrients (Guillard and Hargraves, 1993). All stock cultures were grown
Growth
As shown in Fig. 1, an increase (p = 0.0001) in growth occurred between both CO2 treatments. Cells in the 1000 μatm CO2 treatment reached a growth plateau sooner than controls and showed a significantly larger density at the stationary phase ([2.01 ± 0.07] × 107 cells L−1, p = < 0.01) than in the 395 μatm CO2 treatment ([1.85 ± 0.06] × 107 cells L−1). Growth rates also showed that cells under elevated CO2 concentration grew faster (0.31 ± 0.003 day−1) than controls (0.26 ± 0.03 day−1) during the exponential period.
Discussion
Rise in pollution due to industrial and agricultural chemicals seeping into the environment is the proposed cause for the increase of HABs. In addition, a range of global climate change scenarios is thought to be linked to increasing toxic algal bloom episodes worldwide. In recent decades, the global carbon cycle has been significantly perturbeddue to human intervention. The atmospheric partial pressure of CO2 (pCO2) has risen nearly 40% since 1950, due to the burning of fossil fuels,
Conclusion
In this study, A. tamarense strain ATDH isolated from the East China Sea showed significant increase in growth and cellular toxicity under elevated pCO2 levels. All findings indicate that changes of atmospheric CO2 levels may affect the growth and toxicity of toxicogenic HAB species. For complex processes of ocean acidification, future studies are necessary to assess the effects of acidification. Studies such as these are vital considering the global environmental changes such as rising levels
Acknowledgements
The study was partly supported by the National Natural Science Foundation of China (41606140, 31101875 and 41706140), the National Key Research and Development Program of China (2016YFC1402106 and 2016YFC1402104), and funds from the Key Laboratory for Ecological Environment in Coastal Areas, State Oceanic Administration.[CG]
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