High levels of volatile organic sulfur compounds (VOSCs) have frequently been detected during algae-induced black blooms, which pose an ecological threat to water bodies and their surrounding residents. In this study, aeration was applied to remove the VOSCs after the outbreak of a black bloom. The removal efficiencies under different aeration rates (A1 (0.06 m3-air min−1 m−3), A2 (0.18 m3-air min−1 m−3), and A3 (0.54 m3-air min−1 m−3)) were compared. For treatments A2 and A3, the level of dissolved oxygen (DO) and the oxidation-reduction potential (Eh) increased sharply after 1 h of aeration, and about 70% of the VOSCs were removed from the water columns; however, for treatment A1, the increases in DO and Eh and the rate of removal of VOSCs were slower. The ultimate removal rate of VOSCs was >99% for all the aerated treatments after 24 h. The alteration of the oxidation-reduction conditions, induced by the aeration, could be the primary reason for the removal of the VOSCs. Thus, aeration treatment might be a feasible technique for the removal of VOSCs after the outbreak of black blooms in waterworks and some shallow lakes.
Black blooms, also known as ‘black spots’, ‘black aggregations’, and ‘black water agglomerates’ (Rusch et al. 1998; Lu 2012), have been observed in many lakes and bays (Duval & Ludlam 2001; Yang et al. 2008). Black-blooming waters pose a considerable ecological threat to water ecosystems and their surrounding residents. In 2007, a potable water crisis occurred in the city of Wuxi in China, when water supplied from the water plants became discolored and had a foul odor (Yang et al. 2008; Zhang et al. 2010). An algae-induced black bloom in Lake Taihu, the city's source of potable water, was responsible for the problem, which caused approximately two million inhabitants to suffer a drinking water shortage.
Algae-induced black blooms are now common phenomena in large shallow lakes, such as Lake Taihu and Lake Chaohu in China, during the algal bloom season (Paerl et al. 2011; Duan et al. 2014; Jiang et al. 2014). Black coloration and foul odor are the two characteristics most typical of affected water during black-bloom events. High concentrations of metal sulfides (typically FeS) generated under conditions of low dissolved oxygen (DO; close to 0 mg L−1) and low oxidation-reduction potential (Eh) are the factors that predominantly induce the black coloration (Stahl 1979; Shen et al. 2013). However, high concentrations of volatile organic sulfur compounds (VOSCs), including methanethiol (MTL), dimethyl sulfide (DMS), dimethyl disulfide (DMDS), and dimethyl trisulfide (DMTS) are most responsible for the foul odor of the water, and they have frequently been detected during algae-induced black blooms (Yang et al. 2008; Lu 2012; Lu et al. 2013). Therefore, in the control of black blooms, it is important to consider both the black coloration and the foul odor of the affected water.
Most measures for controlling black blooms focus on the sediment because the black coloration is induced mainly by high levels of Fe2+ and ΣH2S (H2S, HS−, and S2−) accumulated in surface sediments and pore waters (Shen et al. 2013). Sediment dredging (He et al. 2013; Liu et al. 2015) and plow tillage (He 2013) have both proved suitable for controlling the black coloration. However, the foul odor induced by the VOSCs, which was the primary cause of the potable water crisis in Wuxi (Zhang et al. 2010), cannot be controlled by such measures (Liu et al. 2015). Thus, VOSCs continue to pose a significant threat to the aquatic environment during black blooms. These compounds have been studied for decades because of their low odor-threshold concentrations (OTCs) (Kiene & Visscher 1987; Watson 2004), which cause them to affect the smell and taste of drinking water. They generally originate from sulfur-containing amino acids like methionine and cysteine, as well as their derivatives S-methylmethionine and S-methylcysteine, in anoxic environments (Smet et al. 1998; Lomans et al. 2002a; Higgins et al. 2006). However, algae in large shallow lakes in China (e.g., Lake Taihu) contain many sulfur-containing amino acids (Li 2009), which are the primary sources of VOSCs during black blooms (Lu et al. 2013). In the past decade, despite the implementation of various measures (e.g., salvage and pollutant interception) to control algal blooms in China, the elimination of the origin of VSOCs has proven problematic and the bloom status has remained severe (Duan et al. 2014). There are still no effective measures to control VOSCs after the outbreak of an algae-induced black bloom. Therefore, effective measures are required for the removal of VOSCs to protect lake ecosystems and drinking water for local inhabitants. In this study, aeration experiments were used to investigate the removal of VOSCs because they are usually formed in anoxic environments (Lomans et al. 2002a; Higgins et al. 2006; Hu et al. 2007). Pilot studies were performed in a laboratory to compare and evaluate removal efficiency across various treatments.
MATERIALS AND METHODS
Sediment, water, and algae used in the study
Lake Taihu, which is the third largest freshwater lake in China, has a serious pollution problem because of the development of surrounding industrialized cities (Qin et al. 2007). Since the 1980s, large areas of algal bloom have occurred annually in the lake (Duan et al. 2014), with occasional discoveries of resultant algae-induced black blooms (Lu & Ma 2009; Zhang et al. 2010), which pose a considerable threat to both the lake ecosystem and the inhabitants in the surrounding areas. In this study, prior to the experimental treatments, black blooms were simulated in a laboratory using raw sediment, water, and algae samples from Moon Bay in Lake Taihu, which is an area known to be prone to black blooms. The latitude and longitude of the sampling site are 31 °24′37.7″N and 120 °6′9.7″E, respectively. In July 2013, 15 sediment cores were sampled using a gravity corer (Rigo Co. Ltd, Japan; Ø110 mm × L500 mm) and were stored anaerobically in Plexiglas® tubes (Ø110 mm × L500 mm). The overlying water and algae used during the experiments were also sampled from the same site and stored anaerobically in plastic buckets. All sediment cores, together with the overlying water and algae, were transferred immediately to the laboratory without disturbance and treated within 24 h. The sediment cores and water were stored at normal temperatures, while the algae were stored at 4 °C to reduce degradation during transportation.
Four treatments were implemented after the outbreaks of the black blooms developed: control (CK, without treatment), A1, A2, and A3, for which, in the latter three experiments, 1, 3, and 9 L-air min−1 of aeration (corresponding to 0.06, 0.18, and 0.54 m3-air min−1 m−3) was applied in the middle of the water columns. Air-blast aeration was used for the treatments using air blowers (Figure 1) through which the airflow rate was controlled using rotameters (Krohne DK800, Germany). Temperature in the laboratory was maintained at 27 ± 2 °C, approximating the normal temperature of Lake Taihu during the early summer (Hu et al. 2006). All treatments were applied for 24 h to study their effects in removing VOSCs during black blooms.
Water samples were collected from the outlets in the middle of the columns in the laboratory (Figure 1). The water samples were stored in 40 mL brown glass bottles, sealed immediately, and preserved at 4 °C for the analyses of VOSCs and H2S. Samples were collected successively at 0, 1, 2, 3, 5, 8, and 24 h during the aeration treatment. Concurrent with the sampling, the levels of DO and Eh were analyzed using electrodes (Mettler Toledo SG68, Switzerland) placed in the middle of the water columns.
Concentrations of Fe2+ and Fe3+ in the water were analyzed immediately after the sampling using the ferrozine method (Stookey 1970). VOSCs and H2S were analyzed using gas chromatography, which has been used by many other researchers for the detection of VOSCs (Hu et al. 2007; Chen et al. 2010; Lu et al. 2012). In this study, a headspace solid-phase micro-extraction (HS-SPME) procedure, coupled with an Agilent 7890A gas chromatograph (Agilent Technologies, USA), was used for the determination of VOSCs and H2S. Twenty milliliters of water was extracted from each of the samples using a 50/30-μm DVB/carboxen-PDMS fiber (Supelco, No. 57348-U, USA) over 30 min at 65 °C, with agitation at 150 rpm. Separation and determination of the VOSCs were achieved via gas chromatography using a GAS-PRO capillary PLOT column (60 m × 0.32 mm; Agilent Technologies) and a flame photometric detector. The detector was fed with hydrogen, synthesis air, and helium as an auxiliary gas, at rates of 50, 65, and 30 mL min−1, respectively, and maintained at 250 °C. Helium was also used as the carrier gas at a flow rate of 3.0 mL min−1. The gas chromatograph was programmed from 50 (held for 5 min) to 250 °C (25 °C min−1, held for 10 min). Standard curves were obtained using standard solutions purchased from Sigma-Aldrich (USA). The concentrations of VOSCs, with detection limits ranging from 2.2 to 4.0 ng L−1, were determined by comparison with the standard curves.
Pearson's correlation and analysis of variance (ANOVA) with Tukey's test (used to check the differences between the different treatments) were implemented using SPSS® software for Windows® (Version 19.0; IBM, USA). Graphics were generated from the data using Origin® software (Version 8.5; OriginLab, USA).
RESULTS AND DISCUSSION
Changes of DO and Eh
Effect of aeration on H2S
Effect of aeration on VOSCs
Alteration of oxidation-reduction conditions
Anaerobic degradation of sulfur-containing amino acids to form MTL and H2S is the most important mechanism for the formation of VOSCs (Lomans et al. 2002a, 2002b; Higgins et al. 2006). Other VOSCs (i.e., DMS, DMDS, and DMTS) are formed subsequently through the methylation and oxidation of MTL (Chin & Lindsay 1994; Higgins et al. 2006; Lu 2012). Moreover, the formation of MTL via the anaerobic methylation of H2S (Lomans et al. 2002b; Higgins et al. 2006) aggravates the formation of VOSCs. Furthermore, the formation of FeS by Fe2+ and S2− under a reductive environment is the main reason for the black coloration of the water (Shen et al. 2013; Liu et al. 2015). Therefore, the transition of oxidation-reduction conditions in water bodies is crucial for both the control of VOSCs and the elimination of odorous smells and black coloration.
As shown in Figure 2, levels of DO and Eh increased sharply after 1 h of aeration for treatments A2 and A3. Correspondingly, the H2S concentration decreased sharply under these two treatments (Figure 3). However, large variations in the levels of DO and Eh occurred under treatment A1 until after 3–5 and 2–3 h of aeration, respectively. The decrease of H2S under A1 occurred mainly between the second and eighth hours and it stabilized thereafter, concurrent with the stabilization of the DO level. Significant negative correlations (P < 0.01) were found between DO, Eh, and H2S (Table 1). H2S can be oxidized by molecular oxygen (O2), which can be accelerated by catalysts such as Fe3+ (Mansfield et al. 1992). FeS is the main black compound during black blooms, and high levels of Fe2+ can be detected frequently in black-blooming waters (Shen et al. 2011; He et al. 2013; Feng et al. 2014). Fe2+ can be oxidized to Fe3+ and then become a catalyst for the oxidation of H2S (Mansfield et al. 1992; Smet et al. 1998). In this study, the concentrations of Fe2+ and Fe3+ were also measured to verify both the alteration of the oxidation-reduction conditions and the effects on H2S. The oxidation of Fe2+ to Fe3+ occurred mainly during the first hour of aeration under treatments A2 and A3, with concentrations of Fe2+ decreasing from 0.60 ± 0.01 mg L−1 and 0.51 ± 0.02 mg L−1 to 0.21 ± 0.05 mg L−1 and 0.17 ± 0.01 mg L−1, respectively (the concentrations of Fe3+ escalated accordingly). The corresponding change under treatment A1 occurred mainly between the second and third hours of the experiment, with the concentration of Fe2+ changing from 0.42 to 0.26 mg L−1. It is notable that the rate of decrease under A1 was slower than under A2 and A3. These variations are consistent with the changes of DO and Eh. The escalated Fe3+ became the catalyst for the oxidation of H2S (Mansfield et al. 1992), which is why the concentrations of H2S decreased quickly during the first hour of the experiment under treatments A2 and A3, but decreased at a slower rate after the second hour under A1. The decrease in H2S acts to inhibit further formation of VOSCs (Lomans et al. 2002b; Higgins et al. 2006), and therefore the alteration of the oxidation-reduction conditions of the water columns by aeration might be important for the removal of VOSCs.
Significant at the **P < 0.01 level.
Mechanisms and effects of VOSC removal
It was stated in the previous subsection that the oxidation-reduction conditions in a water body could be changed under the aeration treatment. Under an oxidizing environment, MTL can be oxidized to DMDS and then oxidized further to sulfonic acid (Adewuyi & Carmichael 1986; Hwang et al. 1994), and DMS can be oxidized to dimethyl sulfoxide (DMSO) and other compounds (Arsene et al. 1999; Bentley & Chasteen 2004). Therefore, the alteration of the oxidation-reduction conditions (as demonstrated by the trends of development of DO and Eh in this study) is important for the removal of VOSCs. Moreover, significant negative (P < 0.01) correlations were discovered between the VOSCs and both DO and Eh (Table 1).
The duration of a black bloom is usually no more than 2 days, according to our observations of black blooms in numerous shallow lakes. The emergency removal of VOSCs during the 24 h of a black bloom event might be crucial in avoiding a drinking water crisis for local inhabitants and other related ecological disasters. The final removal rate for all the aerated treatments was >99% after 24 h (Figure 5). Therefore, aeration is shown to be feasible for the removal of VOSCs during algae-induced black blooms. High aeration rates, such as those employed under treatments A2 and A3 (i.e., >0.06 m3-air min−1 m−3), could be used in waterworks to overcome accidental malodorous problems associated with drinking water during black blooms. Lower aeration rates (i.e., <0.06 m3-air min−1 m−3) could be used for the removal of VOSCs in black-blooming areas such as small bays in shallow lakes, where black blooms usually occur.
This study focused on the removal of VOSCs from water during algae-induced black blooms in shallow lakes. Air-blast aeration was used to eliminate VOSCs after the outbreak of black blooms. It was demonstrated that DO and Eh levels can be improved remarkably by aeration, leading to a decrease in H2S, which is of considerable importance regarding the elimination of VOSCs and the suppression of black blooms. The alteration of oxidation-reduction conditions could be the most important factor in the removal of VOSCs. Aeration was found to be a feasible measure for the removal of VOSCs during black blooms. Different aeration rates could be used in waterworks and the small bays of shallow lakes to avoid future crises involving drinking water and other ecological disasters.
This study was supported financially by the One-Three-Five Project of Nanjing Institute of Geography and Limnology, CAS (No. Y213518090) and the Comprehensive Management Project for Taihu Water Environment of Jiangsu Province (No. JSZC-G2013-188).