Mechanism of lead bioaccumulation by freshwater algae in the presence of organic acids
Graphical abstract
Introduction
Heavy metals are released into the environment through human activity such as industrialization after which they undergo transformation and circulation until eventually accumulating to high concentrations. Through the food chain, heavy metals pose a serious threat to the environment and humans (Brower et al., 1997). For examples, fed Cu-enriched microalgae reduced survival rate of scallop larvae (Edding and Tala, 1996), and diets including Cd-contaminated D. tertiolecta caused mortality and weight losses of oysters (Wikfors et al., 1994). Unlike many other pollutants, heavy metals cannot be degraded by chemistry or biology. Furthermore, heavy metals have a strong environmental effect including their migration, transformation, enrichment, and toxicity to aquatic organisms. Removing heavy metals from the environment poses a challenge (Khan et al., 2008; White et al., 1995), although using algae to remove low concentrations of heavy metals from a freshwater environment has shown remarkable positive results (Volesky, 1995). However, one of the most influential and concerning factors in the success of heavy metal removal is dissolved organic matter (DOM). The presence and variety of DOM can cause ramifications to the migration, distribution, and bioavailability of heavy metals (Bai et al., 2010; Reimers et al., 1975).
Recently, the ternary complex of DOM–metal–algae has become a topic of interest. Slaveykova et al. (2003) observed a sharp increase in the adsorption amount of Pb on algae in the presence of DOM. Lamelas and Slaveykova (2007) described the above phenomenon as a ternary complex pointing out that it contributed to more than 90% of the total cellular Pb but small contribution to Cu and Cd. This led to the hypothesis of a ternary complex forming condition, that is, the affinity of metal to algal surface should be comparable with that of humic acid to algae. Later research showed that the presence of Pb in the algal cell wall is primarily in a binding state with DOM, which indicated that some heavy metals can form a ternary complex with the adsorption sites on the cell membrane after complexation with DOM (Lamelas et al., 2009). However, the proposed ternary complex is still a speculation. 19F nuclear magnetic resonance spectroscopy and potentiometry were used to confirm that F and Al coexist in a ternary complex (F-Al-L-cell) in the gills of largemouth bass (Wilkinson et al., 1993), which currently is the best evidence for a ternary complex. However, this does not prove the existence of the DOM–metal–algae ternary complex.
Irrespective of whether ternary complex is the proper term, such complexes do exist. When ternary complexes occur, they alter the behavior of heavy metals beyond our previous knowledge of heavy metals, which may pose an increased threat to the aquatic ecosystem through the food chain. However, there are still knowledge gaps in terms of formation conditions and quantitative description of ternary complexes owing to the diversity of DOM and heavy metals and their complex interactions.
Different sources, molecular weights, and functional groups of DOM determine the transportation of heavy metals by living organisms (Nebbioso and Piccolo, 2013; Worms et al., 2006), as well as how they interact with heavy metals. For example, the complexing capacity of DOM to Cu from municipal sludge is weaker than that to Cu from compost. However, the former has fewer hydrophobic groups and could remove more Cu from the soil (Zhou and Wong, 2001). For Cu, Pb, and Cd, sediment-derived humic acid (HA) had a stronger complexing capacity than soil- and wastewater-derived HA (Ghosh and Banerjee, 1997; Kinniburgh et al., 1996). In addition, complexes of low molecular weight DOM with heavy metals could improve the bioavailability of heavy metals, while those of large molecular weight DOM or insoluble organic matter tend to decrease the bioavailability of heavy metals. For instance, DOM of molecular weights less than 1000 Da increased the bioavailability of Cu to lettuce seedlings, while DOM of molecular weights greater than 1000 Da reduced Cu bioavailability (Wang et al., 2010). Malic acid and citric acid, whose molecular weights are less than 200 Da, increased the bioavailability of Cu, while humic acid with 1000 to more than 12,000 Da molecular weight inhibited the bioavailability of Cu (Inaba and Takenaka, 2005). DOM also contains a large number of hydrophilic and hydrophobic groups, such as carboxyl, sulfonate, and amine functional groups (Miranda et al., 2013; Roozegar and Behnam, 2019), which directly affect the characteristics, migration, and transformation behavior of heavy metals in water (Iso et al., 2005; Ross, 1990; Wu and Tanoue, 2001).
Metal types and the interaction between metal and organic ligand also play key roles in the mobility, bioavailability, and toxicity of metals to aquatic organisms (Guo et al., 2001; Laing et al., 2009). The adsorption and internalization of Cu and Cd in the presence of humic acid were almost the same as those in the absence of humic acid, while those of Pb increased in the presence of humic acid (Lamelas et al., 2009). The addition of DOM greatly enhanced Cd uptake by Microcystis aeruginosa compared with that by the control group (Ni et al., 2017). Some DOM reduced the bioavailability of heavy metals, weakening their toxicity (Trenfield et al., 2012). For example, natural DOM reduced Cu accumulation by bacteria and Paramecium caudatum (protozoan), thus, reducing the entry of Cu into the aquatic microbial food chain (Nogueira et al., 2009).
Previously, we performed a comparative study of citric acid (CA), fulvic acid (FA), and HA representing different molecular weights of DOM and found that the adsorption capacity of Pb increased with a decrease in molecular weight (Shi et al., 2017). However, since FA and HA extracted from water were impure, and only their molecular weight range were determined, so the above relationships could not be quantified.
The aim of the study was to verify the formation of a ternary complex of organic acid–Pb–algae, observe the kinetic process of ternary complex formation, and determine a quantitative relationship among DOM, Pb, and algae. Two small molecular weight organic acids (OAs), malic acid (MA) and CA, were selected to quantitatively compare the effect of their carboxyl groups. The results of this study are expected to support the ternary complex theory and provide basic data and parameters for accurate evaluation of the ecological risk of heavy metals.
Section snippets
Reagents and materials
Chlorella pyrenoidosa was purchased from the Institute of Hydrobiology, Chinese Academy of Sciences. Standard solutions of metals (1000 mg L−1) were purchased from the National Institute of Metrology, Beijing, China.
Analytically pure MA (2-hydroxybutyric acid, HOOCCHOHCH2COOH, 134.09 Da) and CA (2-hydroxypropane-1,2,3-tricarboxylic acid, 192.14 Da) were commercially sourced. MA and CA have simple structures of straight alkanes and both have a hydroxyl group, but each contains a different number
Concentration of dipotassium hydrogen phosphate in BG11 culture medium
Dipotassium hydrogen phosphate (K2HPO4, 40 mg L−1) is an important component of the BG11 culture medium and positively affects algal growth and chlorophyll content. However, hydrogen phosphate ions can react with Pb to form a lead hydrogen phosphate precipitate that is deposited on the surface of algae, which can obstruct experimental observations (Ross, 1990; Serra et al., 2010). Therefore, we performed additional experiments using different concentrations of hydrogen phosphate ion to
Conclusions
The effect of malic acid and citric acid on the bioaccumulation of Pb by Chlorella pyrenoidosa was comparatively studied using the equivalent concentration of effective functional groups. Adding OA to the algae–Pb binary system prolonged the adsorption equilibrium time, but it still fitted the pseudo-second-order model. The equivalent concentration of carboxyl group was negatively correlated with the bioaccumulation rate k2 but maintained a positive linear correlation with the maximum
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgment
This study was supported by the National Natural Science Foundation of China (Project numbers: 41977150) and the Natural Science Foundation of Zhejiang province (Project numbers: LY19B070007).
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