Institute of Oceanology, Chinese Academy of Sciences
Article Information
- HE Qiang, WANG Yiyao, LI Ming
- Influences of aeration induced turbulence on growth and competition of Microcystis and Scenedesmus in the presence of sediments with varying particle sizes
- Journal of Oceanology and Limnology, 40(1): 142-152
- http://dx.doi.org/10.1007/s00343-021-0317-5
Article History
- Received Aug. 18, 2020
- accepted in principle Oct. 18, 2020
- accepted for publication Jan. 14, 2021
2 Chengdu Environmental Protection Research Institute, Chengdu 610072, China
Cyanobacterial blooms, especially Microcystis blooms, is a major water environmental issue around the world (Jacoby et al., 2000; Paerl and Otten, 2013). Artificial mixing such as aeration has been used as a measure to prevent cyanobacterial blooms in eutrophic lakes and reservoirs for many years (Visser et al., 2016). Lehman (2014) demonstrated that a shift from cyanobacteria to green algae was often found in lakes after long-term aeration, thus the cyanobacterial blooms was controlled. However, the utilization of aeration for cyanobacterial blooms management has not always been successful. It was identified that there were no significant effects of aeration on the cyanobacterial blooms in Lake Yogo (Japan) and Lake Sheldon (the United States) (Oberholster et al., 2006; Tsukada et al., 2006). Therefore, it is still required to further understand the mechanisms of cyanobacteria control using aeration, which will effectively guide the implementation of aeration for water environments management.
Aeration and agitation can affect the growth and physiology of algae by means of changing the hydrodynamic conditions (Sitanggang and Lynett, 2010; Fouxon and Leshansky, 2015; Sengupta et al., 2017). As a microcosmic index to directly evaluate the turbulence intensity, the turbulence dissipation rate can effectively reflect the magnitude of hydrodynamic conditions. Li et al. (2017) demonstrated that turbulence promoted the growth of Aphanizomenon flos-aquae when the turbulent dissipation rate increased from 0 to 0.022 59 m2/s3 but was inhibited when the value increased to 0.050 58 m2/s3. Xiao et al. (2016) found that the growth rate of Anabaena flos-aquae increased firstly and then decreased when the turbulent dissipation rate increased from 0 to 8.01×10-2 m2/s3. They also found that the growth rate of Anabaena flos-aquae reached its maximum value when the turbulent dissipation rate was 2.26×10-2 m2/s3. O'Brien et al. (2004) reported a similar phenomenon and the critical turbulent dissipation rate to Microcystis aeruginosa was 7×10-6 m2/s3. Song et al. (2018) found that the superoxide dismutase (SOD) and catalase (CAT) activities of Microcystis were lower at the lower energy dissipation rate compared to those at the higher energy dissipation rate. All the above results indicated that the increase of turbulence intensity firstly promoted the algal growth and then inhibited the growth of algae.
Turbulence may also change phytoplankton community composition (Jungo et al., 2001; Zhu et al., 2013; Barton et al., 2014). Heo and Kim (2004) found that cyanobacteria were replaced by diatoms after aeration in Lake Dalbang (South Korea). Becker et al. (2006) found a decline of cyanobacteria and the increase of green algae and diatoms in Bleiloch reservoir (Germany) when treated with aeration. However, these studies did not provide insight into the turbulence on competition among various phytoplankton. In addition, Huisman et al. (2004) showed that turbulence would affect the competitive relationship between cyanobacteria and green algae and indicated that cyanobacteria dominated under the condition of low turbulence intensity, but the effects of sediment were not considered.
Artificial mixing would inevitably cause the suspension of sediment (Schallenberg and Burns, 2004; Matisoff et al., 2017). Suspended sediment directly affects the light intensity in water, thus affecting the growth and the competition of phytoplankton. Watermann et al. (1999) found that sediment in the range of 63–200 μm promoted the growth of Microcoleus chthonoplastes while the sediment smaller than 63 μm showed an inhibitory effect. Brasil et al. (2018) found that Cylindrospermopsis raciborskii could grow in the suspension of kaolinite and bentonite with particle sizes of 7.5 μm and 10.3 μm, respectively, and the growth rate in the kaolinite suspension was higher than that in the bentonite suspension. Since both kaolinite and bentonite are similar to the solid particles of sediment, it is assumed that sediment particle size may have comparable influence on algae. However, our knowledge about the effects of sediment particle size on the growth of phytoplankton is still limited.
The aim of this study was to understand the effects of turbulence on the growth and the competition of phytoplankton in the presence of sediments with varying particle sizes. In this study, Microcystis aeruginosa and Scenedesmus obliquus were selected as the model organisms. Sediments with varying particle sizes were added into mono and mixed cultures of these organisms. The results may provide effective theoretical guidance to use the aeration for cyanobacteria management.
2 MATERIAL AND METHOD 2.1 Organisms and sedimentUnicellular strains of Microcystis aeruginosa (FACHB-469) and Scenedesmus obliquus (FACHB-416) were purchased from the Institute of Hydrobiology (FACHB collection), Wuhan, Hubei Province, China. Both strains were axenically cultured in BG-11 medium (NaNO3 1 500 mg/L, K2HPO3·3H2O 40 mg/L, MgSO4·7H2O 75 mg/L, CaCl2·2H2O 36 mg/L, Na2CO3 20 mg/L, Ferric citrate 6 mg/L, Na2EDTA·2H2O 1 mg/L, ammonium ferric citrate 6 mg/L, Trace mental solution 1 mg/L, and pH 7) for three months prior to the experiments. The use of BG-11 medium to cultivate cyanobacteria and green algae has been recognized as the most popular method, and the nutrient concentration in BG-11 medium is suitable for the growth of cyanobacteria and green algae. In the experiment, the algae in the maximum growth phase (logarithmic growth period) were selected for inoculation.
Sediment was collected from the Weihe River, in Yangling section of Shaanxi Province, in November 2018. Sediments in the surface layer were collected using Petersen Grab Sampler and were then transferred to the laboratory for our experiments. The chemical properties of sediment are shown in Table 1. The distribution of the sediment particle size was in the range of 0.9–851 μm. Sediment was divided into three groups: small particle size (10–38.5 μm), medium particle size (38.5–75 μm), and large particle size(75–150 μm), which was dried prior to the experiments. The sediments larger than 150 μm were removed using sieves because they were very diffcult to be suspended when treated with mixing. The small size sediment was obtained using a settling column and the others groups were obtained using sieving method. A laser particle size analyzer (2000E, Mastersizer, UK) was used to determine the size distribution of the sediment and the result was shown in Fig. 1a.
2.2 Experimental design and culture conditionsA cylindrical reactor equipped with an aeration device was used for algae cultivation in this study. The cylindrical reactor was a glass tube with an inner diameter of 8 cm and a volume of 1.5 L (Fig. 1b). Both mono and mixed cultures in BG-11 culture medium were treated with aeration and sediment addition. Aeration treatments were carried out in both daytime and nighttime which were mimicked in an incubator and the aeration intensity was divided into low-intensity (0.16 L/min) and high-intensity (1.2 L/min). For every batch experiment, aeration was carried out for 45 min, afterwards, the samples were rested for 15 min. This time interval was allowed for the aerator pump to dissipate heat. For each aeration treatment, sediments in different particle sizes (small, medium, and large) were added. The concentration of dried sediment was adjusted to 500 mg/L.
Both mono and mixed cultures were carried out at 25 ℃ under a 12-h꞉12-h light-dark cycle in BG-11 medium. Light intensity was 50 μmol photons/(m2·s). The initial cell densities of M. aeruginosa and S. obliquus were 10×104 cells/mL. Experiments were conducted for 12 days. Experiments on each treatment were conducted in triplicate.
2.3 Chemical analysisZeaxanthin (Zeax) is usually considered as the characteristic pigment of M. aeruginosa. Lutein (Lut) and chlorophyll b (Chl b) are the characteristic pigments of S. obliquus. Additionally, chlorophyll a (Chl a) is the common pigment for M. aeruginosa and S. obliquus. They were analyzed daily via high performance liquid chromatography (HPLC, Agilent-1100 series, USA) to indicate the biomass of M. aeruginosa and S. obliquus, respectively. In this study, Zeax, Lut, Chl b and Chl a were purchased from Sigma-Aldrich for pigment analysis. Except for the concentration of standard substance Zeax which is 2 mg/L, the concentration of other standard substance pigments is 20 mg/L.
Algae culture of 10 mL was firstly filtrated through a glass fiber membrane (GF/F, Whatman, UK). Then, the filtered membrane was transferred into a 25-mL test tube with a stopper. Injected with 5-mL acetone solution (99.5%), the tube was treated with ultrasound at 4 ℃ for 10 min. The tube was then frozen at -20 ℃ in darkness. Afterwards, the extract liquid was injected into a 1.5-mL brown chromatographic bottle for HPLC analysis. The packing material of chromatographic column is YMC-Triart C18/S-5 μC/ 12 nm, and the flow rate is 1.00 mL/min. The HPLC elution was conducted as per the procedure suggested by Tian et al. (2019).
2.4 Assessment of turbulence intensityThe turbulent dissipation rate is a direct indicator to evaluate the intensity of turbulence, which can avoid the influence of the reactors on the test results. Significantly different turbulent intensities could be induced by the same aeration intensity when the reactors are different. Computational fluid dynamics (CFD) model was used to calculate the turbulent dissipation rate in the reactors treated with different aeration intensities. The CFD model was constructed according to the method described by Feng et al. (2020). In this study, the turbulent dissipation rates of the experimental apparatus were 1.60×10-6 and 1.16×10-5 m2/s3 corresponding to the low-intensity and high-intensity aerations.
2.5 Statistical analysisThe inhibition rate caused by sediment in monoculture was calculated according to Eq.1:
The biomass of M. aeruginosa and S. obliquus in the monoculture, without sediment addition, aerated during the daytime was selected as the control for each treatment. In Eq.1, K0 and r0 represent the carrying capacity and the intrinsic growth rate of control, respectively. Nn, Nn–1, and N1 represent the abundances of algal biomass with other treatment at tn, tn–1, and t1 (days), respectively.
A Lotka-Volterra's competition model was conducted to assess the effects of sediment and aeration on the competition between M. aeruginosa and S. obliquus. The method was described in our previous work (Zhao et al., 2021). The significance was assessed using one-way ANOVA (P<0.05).
3 RESULT 3.1 Growth curves of M.aeruginosa and S.obliquus in monocultureIn the absence of sediment, the biomass of M. aeruginosa under low-intensity aeration was higher than that under high-intensity aeration (Fig. 2). However, there was no significant difference in the biomass of S. obliquus under different aeration intensities (Fig. 3).
Under the conditions of small, medium, and large size and sediments low-intensity aeration during the daytime, the biomass of M. aeruginosa was the largest, with 2.00, 2.42, and 2.65 mg/L, respectively. The biomass of M. aeruginosa under low-intensity aeration was higher than that under high-intensity aeration for all sizes of sediment. However, there was no significant difference in the biomass of S. obliquus under different aeration modes. Compared with the absence of sediment, the biomasses of M. aeruginosa and S. obliquus were the lowest under the aeration mode with small size sediment.
3.2 Growth curves of M. aeruginosa and S. obliquus in mixed cultureIn the absence of sediment, there was no significant difference in the biomass of M. aeruginosa under different aeration intensities. The biomass of S. obliquus under low-intensity aeration was greater than that of high-intensity aeration in the daytime (Fig. 4), while the biomass under high-intensity aeration was higher than that of low-intensity aeration in the nighttime (Fig. 5).
In the presence of small, medium, and large size sediments, there was no significant difference in the biomass of M. aeruginosa under different aeration modes. However, the biomass of S. obliquus under low-intensity aeration was greater than that of high-intensity aeration in the daytime. The results were just the reversed in the nighttime. The biomass of M. aeruginosa was much lower than that of S. obliquus under different aeration modes.
3.3 Inhibition rates of M. aeruginosa and S. obliquus in monocultureRegardless of the presence of sediment, the inhibition rate of M. aeruginosa under low-intensity aeration was greater than that under high-intensity aeration. With the small size sediment addition, the inhibition rate of M. aeruginosa was the highest with the low-intensity aeration in the nighttime, which was 89.2% (Fig. 6a). The inhibition rate of S. obliquus was negative under various treatments, indicating a certain promotion effect (Fig. 6b).
3.4 Competition coeffcient of M. aeruginosa and S. obliquus in mixed cultureIn the absence of sediment, competition coeffcient α (S. obliquus against M. aeruginosa) decreased with the increase of aeration intensity, but β (M. aeruginosa against S. obliquus) did not change with the increase of aeration intensity. The growth of M. aeruginosa was inhibited by S. obliquus under low-intensity aeration, but there was no inhibition effect between M. aeruginosa and S. obliquus under high-intensity aeration (Fig. 7).
In the presence of small, medium, and large size sediment, the growth of M. aeruginosa was significantly inhibited by S. obliquus under low-intensity aeration, which was higher than that cultured without sediment. The maximum competition coeffcient was 12.1 when the small size sediment was aerated in the daytime. There was no inhibition effect between M. aeruginosa and S. obliquus under high-intensity aeration.
4 DISCUSSIONOur results show that aeration inhibited the growth of M. aeruginosa but promoted the growth of S. obliquus. This phenomenon indicated that the tolerance of Scenedesmus to the turbulence was higher than that of Microcystis. Species-specific tolerance to turbulence was also reported by Hondzo and Wüest (2009). Thomas and Gibson (1990) reported that cyanobacteria was more sensitive to turbulence than other algae. Yu et al. (2018) found that the green algae Chlorella was superior to the cyanobacteria Microcystis in highly turbulent water environments. Mitsuhashi et al. (1995) showed that the differences in size and shape of algal cells would lead to variations in algal nutrient transport in turbulent water and thus affecting the algal growth. Algae with larger cell size may have higher tolerance to turbulence (Cross et al., 2014). The cell size of Microcystis was much lower than that of Scenedesmus and Chlorella. This could be the main reason that Microcystis was less resistant to turbulence compared to Scenedesmus.
Turbulence generated by aeration can directly affect algal growth by producing shear stress but can also indirectly influence algal growth by changing the light and nutrient resources available to the algae (Chengala et al., 2013; Wilkinson et al., 2016). Moderate intensity turbulence promoted algal growth principally because turbulence motivated the exchange of the upper and lower layers of the water body, so that algae can get more light and uptake more nutrient (Warnaars and Hondzo, 2006). Moreover, the locally higher concentration of metabolites around the algae was also reduced (Grobbelaar, 1994).However, high intensity turbulence produced shear stress which may cause mechanical damage to algae and thus inhibit algal growth (Hondzo and Lyn, 1999; Barbosa et al., 2004; Michels et al., 2016).
On the other hand, aeration also provided more carbon dioxide which was essential for algal photosynthesis (Gao et al., 1999). In the daytime, the carbon dioxide provided by aeration could be used directly for algal photosynthesis (Qiu and Gao, 2002), but the carbon dioxide was unlikely to be used in the nighttime (Harvey and Macko, 1997). Compared with daytime, the inhibitory effect of aeration in the nighttime on Microcystis and the promotion to Scenedesmus in the monoculture were stronger. Nevertheless, the growth of Microcystis was also inhibited by aeration in the daytime. At this time, carbon dioxide provided by aeration may promote the growth of Microcystis to a certain degree, but the overall effect was inhibition. The inhibition rate of aeration in the nighttime to Scenedesmus was greater than that in the daytime. This may be due to the facultative heterotrophic ability of Scenedesmus, which means Scenedesmus can grow well using organic carbon sources in darkness (Liang et al., 2009; Heredia-Arroyo et al., 2011).
Several studies have reported that sediment in water environments could affect algal biomass by means of influencing light attenuation and adsorbing nutrients (Guenther and Bozelli, 2004; Schallenberg and Burns, 2004; Effler et al., 2012). He et al. (2017) demonstrated that sediment affected algal growth by adsorbing or releasing nutrients. Kang et al. (2019) found that sediment could inhibit algal photosynthesis by reducing light intensity. In the current study, there was no obvious difference in the growth of both M. aeruginosa and S. obliquus between the daytime and nighttime treatments with sediment addition. This phenomenon indicated that sediments merely reduced the light intensity, and subsequently affected algal growth in the current study. In monocultures, the inhibition rate of M. aeruginosa decreased with the increase of sediment particle size when treated with low-intensity aeration in the nighttime. The reason could be that the sediments with larger particle size were more prone to attenuate turbulence intensity at microscale.
Some studies indicated that turbulence affected the phytoplankton communities. The dominant species changed from cyanobacteria to green algae or diatoms when a lake was treated with aeration (Visser et al., 1996; Qu et al., 2018). This was mainly attributed to the fact that the turbulence reduced the floating advantage of cyanobacteria (Oliver, 1994; Huisman et al., 2004). The current study found that the growth of M. aeruginosa was inhibited by S. obliquus when treated with aeration, which was consistent with the previous studies (Zhou et al., 2016).
5 CONCLUSIONOur results demonstrate that Scenedesmus was more resistant to the turbulence than Microcystis in monocultures. In the presence of sediment, S. obliquus was promoted, while M. aeruginosa was inhibited under all aeration conditions. The highest inhibition rate of M. aeruginosa was identified under the condition of low-intensity aeration in the nighttime with small sediment addition, which was 89.2%. Our results indicated that aeration induced turbulence could be used to mitigate the harmful algal blooms, particularly under the small sediment particle size condition. Furthermore, our results indicated that sediments had insignificant effect on the algal growth by reducing the light intensity. Artificial mixing could be an effective measure to promote a shift in phytoplankton composition from cyanobacteria to green algae. Our results provided a theoretical guidance to use the aeration for cyanobacteria management. It is also suggested that the field study of variation in phytoplankton community caused by the artificial mixing should be undertaken in the future.
6 DATA AVAILABILITY STATEMENTData are available upon reasonable request from the authors.
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