Berberine is a potent algicidal allelochemical of Microcystis aeruginosa. To optimize its application in the control of Microcystis blooms, the effects of berberine on the growth and photosynthetic activities of M. aeruginosa and a non-target green alga, Chlorella pyrenoidosa, were compared. The results showed that the algicidal activity of berberine on M. aeruginosa was light dependent. Berberine had no algicidal effects on C. pyrenoidosa with or without light exposure. Under light-dark conditions, berberine significantly decreased the chlorophyll fluorescence parameters in M. aeruginosa while no significant berberine-induced changes were observed under constant darkness. Significant reductions of photosystem II (PSII) and whole chain electron transport activities in M. aeruginosa exposed to berberine suggested that PSII was the important target site attacked by berberine. Contrary to M. aeruginosa, no berberine-induced inhibition in photosynthesis activities were observed in C. pyrenoidosa. The differences in photosynthetic apparatuses of these two algae might be responsible for their different sensitivities to berberine.

Cyanobacterial blooms and their adverse effect on aquatic ecosystems and human health have been reported worldwide, and create an urgent need for their monitoring and control (Codd et al. 2005; O'Neil et al. 2012; Ma et al. 2016). Cyanobacteria produce toxic metabolites, which are usually classified as dermatotoxins, neurotoxins, and hepatotoxins according to the toxic effects on animals. Microcystins are hepatotoxins to which special attention has been given, not only due to their ability to cause acute poisoning but also due to their cancer promoting potential through the chronic exposure of humans (de Figueiredo et al. 2004). Controlling cyanobacterial blooms has become an urgent issue worldwide because of its increasing occurrence (Ni et al. 2012; Lu et al. 2014; Lei et al. 2018; Page et al. 2018).

Among physical, chemical, and biological measures proposed, allelopathy has been considered as one of the most promising biological algal control technologies for its higher environmental safety (Shao et al. 2013; Yang et al. 2013). Allelopathic effects of exudates of one aquatic organism on the other one are rather common, but only a fraction of compounds responsible for these effects can potentially be used in controlling growth; some allelochemicals are likely to change a variety of physiological processes of cyanobacteria, such as photosynthesis, respiration, gene expression and enzyme function (Dziga et al. 2007; Shao et al. 2009; Zhu et al. 2010; Huang et al. 2015). It has been reported that the photosystem of phytoplankton is probably an important target of some allelochemicals (Zhu et al. 2010).

Microcystis aeruginosa is responsible for approx. 70–75% of freshwater blooms. (Azevedo et al. 2002; Wu et al. 2007; Steffen et al. 2014). In a previous study, it was found that golden thread (Coptis chinensis) could significantly inhibit M. aeruginosa growth and berberine was the main bactericidal chemical of golden thread (Zhang et al. 2010). A subsequent study indicated that berberine had no sterilizing effects on M. aeruginosa without light exposure (Zhang et al. 2013). Based on its light-dependent sterilizing effects on M. aeruginosa, we speculated that berberine might be a photosynthesis-inhibiting algicidal allelochemical. However, the target sites in the photosystem attacked by berberine remained unknown.

Application of algicides, such as metals, photosensitizers, and herbicides, has been developed as the ‘acute’ treatment for the control of cyanobacterial blooms (Costas & Lopez-Rodas 2006; Jančula & Maršálek 2011). Cylindrospermopsin has been shown to control the growth of M. aeruginosa, and even inhibit microcystin production by intact cells (Rzymski et al. 2014). However, cylindrospermopsin itself is a toxin so one cannot rely on this compound in environmental management. Although some algicides are effective within a short period after application, their usage is potentially dangerous because of the threat to environmental safety and lack of selectivity (Jančula & Maršálek 2011; Walker 2017; Zhang et al. 2019). Most algicides do not selectively target harmful cyanobacteria in aquatic environments, and thus non-harmful algae may also be eliminated or negatively affected simultaneously.

It has been found that various algal species show different tolerance to some photosynthesis-inhibiting herbicides (Peterson et al. 1997; Fairchild et al. 1998). Pollution by a photosynthesis-inhibiting herbicide in aquatic environments could affect the competitive battle between susceptible algae and tolerant ones, thereby inducing changes in algal community structure (Lürling & Roessink 2006). As berberine might be a photosynthesis-inhibiting algicidal allelochemical, comparing the sensitivities of M. aeruginosa and non-target algae to berberine will benefit the application strategy of berberine in cyanobacterial bloom control.

In this study, to reveal whether or not berberine can be used selectively to target M. aeruginosa, we compared the effects of berberine on the growth of the cyanobacteria M. aeruginosa and the non-harmful green alga Chlorella pyrenoidosa with and without light exposure. In addition, changes in photosynthetic activities were also investigated to reveal the target sites of M. aeruginosa for berberine attack, and elucidate the algicidal mechanism involved. The results provide insights for the optimal application of berberine in cyanobacterial blooms control.

Algal cultures

M. aeruginosa (FACHB-905), a microcystin producing strain, and C. pyrenoidosa were provided by the Institute of Hydrobiology, Chinese Academy of Sciences. Algae were cultured in sterilized BG11 medium containing (g/L): NaNO3, 1.5; K2HPO4, 0.04; MgSO4•7H2O, 0.075; CaCl2•2H2O, 0.036; citric acid, 0.006; iron (III) ammonium citrate, 0.006; Na2-EDTA, 0.001; and Na2CO3, 0.02; and 1 mL of trace element solution (mg/L): H3BO3, 61; MnSO4•H2O, 169; ZnSO4•7H2O, 287; CuSO4•5H2O, 2.5; and (NH4)6Mo7O24•4H2O, 12.5; at pH 7.4 (Rippka et al. 1979), under light-dark conditions (12:12 LD cycle) with a light density of 40 μmol photons/m2/s at 25 °C. M. aeruginosa and C. pyrenoidosa from the exponential growth phase were used for the subsequent experiment.

Berberine treatment

Berberine stock solution (10%, w/v) prepared by dissolving hydrochloride berberine (Northeast General Pharmaceutical Factory, China) in heated distilled water was added to the algal cultures of M. aeruginosa (3.99 × 106 ind/ml) and C. pyrenoidosa (4.04 × 106 ind/ml), respectively. The final concentration of berberine was 4 mg/L, and algal cultures without berberine addition were used as the controls. All treatments were done in triplicate. The algae were cultured in sterilized BG11 medium at 25 °C under light-dark conditions (40 μmol photons/m2/s, 12:12 LD cycle) or constant dark conditions for 9 days. Samples were removed from the cultures at 24-hour intervals to observe the changes in cell densities and chlorophyll fluorescence parameters. Moreover, under light-dark conditions, the chlorophyll fluorescence parameters of M. aeruginosa were measured at 2-hour intervals in the first 10 hours of light exposure.

Measurement of algal cell density and chlorophyll fluorescence parameters

The algal densities were examined with a haemacytometer (Improved Neubauer Counting Chamber) under a microscope. The chlorophyll fluorescence parameters of M. aeruginosa and C. pyrenoidosa were measured using a PHYTO-PAM phytoplankton analyzer (Walz, Germany). The maximum relative photosynthetic electron transport rate (ETR) values could be read directly, and the maximum PSII quantum yield (Fv/Fm) could be calculated according to the following formula (Campbell et al. 1998):
formula
where Fo was the minimum fluorescence yield in the dark-adapted state, and Fm was the maximum PSII fluorescence yield achieved by illuminating algae under a light intensity of 3,500 μmol photons/m2/s for 0.7 seconds.

Measurement of dark respiration, photosynthetic O2 evolution and electron transport activities

The 50% inhibition concentration (EC50) of berberine was determined based on the cell densities of M. aeruginosa exposed to berberine for 24 hours: the 24 h-EC50 value of berberine on M. aeruginosa was 0.47 mg/L. As the dosage of berberine used in the current study had no inhibitory effects on the growth of C. pyrenoidosa and therefore the 24 h-EC50 value could not be determined, both M. aeruginosa and C. pyrenoidosa were treated with 0 (control) and 0.47 mg/L berberine for 24 hours. Chlorophyll a (Chl a) was determined spectrophotometrically at 647 and 664.5 nm according to the method of Inskeep & Bloom (1985). After being harvested by centrifugation and resuspended in BG11 medium with or without 0.47 mg/L berberine addition (control), algal photosynthetic O2 evolution and electron transport activities were assayed using a Clark type oxygen electrode (Hansatech, UK) at 950 μmol photons/m2/s and 25 °C according to the method of Chen et al. (2007). Dark respiration was estimated from the O2 consumed in darkness. The true photosynthesis rate was equivalent to the sum of O2 evolution and consumption in dark respiration.

PSII electron transport activities were determined based on O2 evolution in the assay mixture comprising 25 mM bis-tris propane (BTP, pH 7.8) and 1 mM p-benzoquinone (p-BQ). PSI electron transport activities were determined by O2 consumption in the assay mixture containing 25 mM BTP (pH 7.8), 0.1 mM 2,6-dichlorophenol indophenol (DCPIP), 5 mM ascorbate (ASC) to reduce DCPIP to DCPIPH2, 0.1 mM methyl viologen (MV), 1 mM NaN3 and 10 μM 3-(3,4 dichlorophenyl)-1, 1-dimethyl urea (DCMU). Whole electron chain transport activities were estimated in terms of O2 consumption in the assay mixture containing 25 mM BTP (pH 7.8), 1 mM NaN3 and 0.1 mM MV. Inhibitors, electron donors and acceptors used in the measurement of electron transport activities are shown in Table 1.

Table 1

Inhibitors, electron donors and acceptors used in the measurement of electron transport activities

Electron donorElectron acceptorRespiration inhibitorPSII activity inhibitor
Whole chain H2MV NaN3  
PSI DCPIP MV NaN3 DCMU 
PSII H2p-BQ   
Electron donorElectron acceptorRespiration inhibitorPSII activity inhibitor
Whole chain H2MV NaN3  
PSI DCPIP MV NaN3 DCMU 
PSII H2p-BQ   

Abbreviations: MV, methyl viologen; DCPIP, 2,6-dichlorophenol indophenol; p-BQ, p-benzoquinone; DCMU, 3-(3,4 dichlorophenyl)-1,1-dimethyl urea.

Statistical analysis

Data are expressed as means ± SD and the t-test was used to evaluate the statistical significance of differences between controls and treatments. Values of P < 0.05 were considered to indicate significance.

Effects of berberine on the growth of M. aeruginosa and C. pyrenoidosa

As shown in Figure 1(a), under light-dark conditions, 4 mg/L berberine could eliminate M. aeruginosa effectively and the cell density dropped to zero on day 6. By contrast, berberine exhibited no sterilizing effects on M. aeruginosa under constant darkness. As shown in Figure 1(b), whether under normal light-dark conditions or constant dark conditions, there was no significant difference between cell densities of C. pyrenoidosa with and without berberine exposure (P > 0.05), suggesting that berberine had no algicidal activity on C. pyrenoidosa.

Figure 1

Effects of berberine on the growth of M. aeruginosa (a) and C. pyrenoidosa (b) with or without light exposure. LD stands for light-dark conditions (40 μmol photons m−2 s−1, 12:12 LD cycle); D stands for constant dark conditions; B stands for berberine. Data are the mean ± SD (n = 3).

Figure 1

Effects of berberine on the growth of M. aeruginosa (a) and C. pyrenoidosa (b) with or without light exposure. LD stands for light-dark conditions (40 μmol photons m−2 s−1, 12:12 LD cycle); D stands for constant dark conditions; B stands for berberine. Data are the mean ± SD (n = 3).

Figure 2

Effects of berberine on the chlorophyll fluorescence parameters of M. aeruginosa (a) and C. pyrenoidosa (b) with or without light exposure. LD stands for light-dark conditions (40 μmol photons m−2 s−1, 12:12 LD cycle); D stands for constant dark conditions; B stands for berberine. Data are the mean ± SD (n = 3).

Figure 2

Effects of berberine on the chlorophyll fluorescence parameters of M. aeruginosa (a) and C. pyrenoidosa (b) with or without light exposure. LD stands for light-dark conditions (40 μmol photons m−2 s−1, 12:12 LD cycle); D stands for constant dark conditions; B stands for berberine. Data are the mean ± SD (n = 3).

Effects of berberine on chlorophyll fluorescence parameters of M. aeruginosa and C. pyrenoidosa

Changes in the chlorophyll fluorescence parameters of M. aeruginosa exposed to berberine are shown in Figure 2(a). Compared to M. aeruginosa without berberine exposure, 4 mg/L berberine significantly decreased Fv/Fm and ETR under light-dark conditions (P < 0.05). After being exposed to berberine for 1 day, Fv/Fm and ETR of M. aeruginosa dropped to nearly zero or zero. Under constant darkness, there were no significant differences in Fv/Fm and ETR between M. aeruginosa with and without berberine exposure (P > 0.05). The measurement of the chlorophyll fluorescence parameters was performed in the light, which might be responsible for berberine-induced insignificant decreases in Fv/Fm and ETR of M. aeruginosa. Consistent with the growth performance of C. pyrenoidosa, no berberine-induced changes in both Fv/Fm and ETR of C. pyrenoidosa were observed under light-dark and constant dark conditions (Figure 2(b)). Under constant darkness, the chlorophyll fluorescence parameters of both M. aeruginosa and C. pyrenoidosa decreased with the prolongation of culture time.

As shown in Figure 3, compared to the control group, berberine decreased Fv/Fm and ETR significantly for M. aeruginosa in the first 10 hours under light conditions (P < 0.05). After 10 hours of exposure to berberine, Fv/Fm and ETR dropped to 0.04 and 0 μmol electrons/m2/s, respectively.

Figure 3

Changes in the chlorophyll fluorescence parameters of M. aeruginosa during the first 10 hours of berberine exposure under light conditions (40 μmol photons m−2 s−1). Data are the mean ± SD (n = 3).

Figure 3

Changes in the chlorophyll fluorescence parameters of M. aeruginosa during the first 10 hours of berberine exposure under light conditions (40 μmol photons m−2 s−1). Data are the mean ± SD (n = 3).

Effects of berberine on the dark respiration, photosynthetic oxygen evolution and electron transport activities of M. aeruginosa and C. pyrenoidosa

As shown in Table 2, 0.47 mg/L berberine inhibited the true photosynthesis rate of M. aeruginosa significantly (P < 0.05). However, the dark respiration rate was not significantly affected by 0.47 mg/L berberine treatment (P > 0.05). Compared to the control, no significant changes were observed in the true photosynthesis rate and dark respiration rate of C. pyrenoidosa exposed to 0.47 mg/L berberine (P > 0.05).

Table 2

Effects of 0.47 mol/L berberine on the dark respiration, true photosynthesis and electron transport activities of M. aeruginosa and C. pyrenoidosa

Rate (μmol O2/mg Chl a/h)M. aeruginosa
C. pyrenoidosa
Control0.47 mg/L berberineControl0.47 mg/L berberine
Dark respiration 49.52 ± 4.36 41.93 ± 4.87 21.40 ± 0.34 22.83 ± 1.55 
True photosynthesis 131.20 ± 8.86 107.82 ± 7.80* 357.83 ± 68.06 336.20 ± 43.83 
Whole chain activity 107.93 ± 6.54 78.02 ± 14.55* 185.36 ± 9.50 190.85 ± 26.30 
PSII activity 186.52 ± 7.91 80.94 ± 9.39** 185.36 ± 23.24 189.44 ± 30.17 
PSI activity 43.89 ± 9.81 47.89 ± 10.03 343.24 ± 80.31 312.49 ± 31.95 
Rate (μmol O2/mg Chl a/h)M. aeruginosa
C. pyrenoidosa
Control0.47 mg/L berberineControl0.47 mg/L berberine
Dark respiration 49.52 ± 4.36 41.93 ± 4.87 21.40 ± 0.34 22.83 ± 1.55 
True photosynthesis 131.20 ± 8.86 107.82 ± 7.80* 357.83 ± 68.06 336.20 ± 43.83 
Whole chain activity 107.93 ± 6.54 78.02 ± 14.55* 185.36 ± 9.50 190.85 ± 26.30 
PSII activity 186.52 ± 7.91 80.94 ± 9.39** 185.36 ± 23.24 189.44 ± 30.17 
PSI activity 43.89 ± 9.81 47.89 ± 10.03 343.24 ± 80.31 312.49 ± 31.95 

Data are the mean ± SD (n = 3) and are marked with asterisk(s) when significantly different (*P < 0.05; **P < 0.01) compared to the rate in the control.

After being treated with 0.47 mg/L berberine, the whole chain electron transport activity and PSII electron transport activity of M. aeruginosa were significantly decreased by 28% and 57%, respectively (P < 0.05; P < 0.01). However, 0.47 mg/L berberine did not affect the PSI electron transport activity of M. aeruginosa significantly (P > 0.05). No significant difference in the photosynthetic electron transport activities of C. pyrenoidosa were observed in the presence or absence of 0.47 mg/L berberine (P > 0.05).

M. aeruginosa, as a photoautotroph species, relies heavily on its photosynthetic systems for energy conversion, which is also the main target of allelopathic substances (Dziga et al. 2007; Shao et al. 2011). The light-dependent algicidal effects of berberine on M. aeruginosa indicated that berberine might be a photosynthesis-inhibiting algicidal allelochemical. Chlorophyll fluorescence has been proven to be useful for indicating the changes in photosynthesis under stress conditions (Vonshak et al. 2001; Deng et al. 2015). Berberine could noticeably decrease the chlorophyll fluorescence parameters in M. aeruginosa after short-term light exposure, which decreased sooner and more rapidly than the cell density. This is consistent with the previous research results of Rzymski et al. (2013), that the fluorescence changes of M. aeruginosa can be preceded by changes in cell density when cells are exposed to toxic metals. Changes in the chlorophyll fluorescence further support our previous speculation that berberine could eliminate M. aeruginosa by inhibiting photosynthesis.

The many reactions that occur during photosynthesis in plants can be grouped into two broad categories: the photosynthetic electron-transfer reactions (also called the ‘light reactions’) in the thylakoid and the carbon-fixation reactions (also called the ‘dark reactions’) in the stroma (Alberts et al. 2002). The formation of ATP, NADPH, and O2 in the photosynthetic electron-transfer reactions requires light energy directly (Trebst 2003), and two photosystems (PSI and PSII) are responsible for converting light energy into redox processes (Lunde et al. 2000; Rast et al. 2015). The interruption of electron flow in PSII or diversion of electrons in PSI are the main targets for some photosynthesis-inhibiting herbicides and phytotoxins (Leu et al. 2002; Muller et al. 2008; Dayan & Zaccaro 2012; Deng et al. 2015). Some commercial photosynthesis-inhibiting herbicides, such as diuron and atrazine, are PSII inhibitors: they compete with the binding of plastoquinone at its BQ binding site and inhibit energy transfer. Other herbicides, such as paraquat, act on PSI (Dayan & Zaccaro 2012).

PSII reaction centers, as the main photosynthetic apparatus, play a key role in photosynthesis in cyanobacteria (Ou et al. 2012). It is more susceptible to various environmental stresses than PSI (Singh et al. 2012). For algicidal allelochemicals, Zhu et al. (2010) found pyrogallic acid and gallic acid could reduce photosynthetic activity in M. aeruginosa and PSII in cyanobacteria was considered to be one of the target sites attacked by allelopathic polyphenols. In the present study, berberine could significantly inhibit PSII electron transport activity in M. aeruginosa while no significant changes in PSI electron transport activity were observed, suggesting the targeted action sites of berberine are located on the electron transport chain PSII of M. aeruginosa.

Berberine could eliminate M. aeruginosa effectively by interrupting the electron flow on PSII but had no algicidal effects on C. pyrenoidosa. No berberine-induced inhibition in photosynthesis and electron transport activities were observed in C. pyrenoidosa. A possible explanation for the different sensitivities might be related to the different cell structures of these two algae. Zhu et al. (2010) found that the opposite inhibitory effects of allelopathic polyphenols on M. aeruginosa and Selenastrum capricornutum might be due to the different photosynthetic apparatuses in cyanobacteria and chlorophytes (Zhu et al. 2010). The cyanobacteria Microcystis are phototrophic prokaryotes, and their photosynthetic thylakoids are directly exposed to the cytoplasm (Stanier & Cohen-Bazire 1977). In contrast to cyanobacteria, photosynthetic thylakoids in phototrophic eukaryotic algae are enclosed by chloroplast envelope consisting of a double membrane, a highly permeable outer membrane and a much less permeable inner membrane (Amils 2011). The inner membrane of the chloroplast has a selective permeability, reflecting the presence of specific carrier proteins (Alberts et al. 2002). It's worth mentioning that M. aeruginosa, as a kind of bacteria, is more sensitive to berberine as an antibacterial agent, while C. pyrenoidosa, as a eukaryote, is not sensitive to it (Čerňáková & Košťálová 2002). The permeability status of the chloroplast membrane to berberine could play an important role in mediating its algicidal activity in eukaryotic algae. Because there were changes in the photosynthetic activity of C. pyrenoidosa, we speculated that berberine might have no opportunity to permeate through the inner membrane of its chloroplast, leading to no disturbance in photosynthesis. This might be the reason why berberine had no algicidal effects on C. pyrenoidosa. To maximize the benefits of using berberine to control cyanobacterial blooms, the toxicity of berberine to more target cyanobacteria species and more non-target algal species needs to be studied. Studies have reported that berberine can have some beneficial effects on other aquatic animals, such as farmed fish, including inhibiting fish oxidative stress, enhancing fish immunity, and reducing fatty liver and diseases (Chen et al. 2016; Zhou et al. 2018).

Finally, it is worth noting that berberine-induced lysis of toxic Microcystis will release microcystins into the surrounding water and result in the rapid increase of microcystin concentrations in the water column. To avoid the potential threats from microcystins, it is important to eliminate them using effective measures, such as biodegradation, photodegradation, ozonation and activated carbon adsorption.

As a photosynthesis-inhibiting allelochemical, berberine could eliminate M. aeruginosa effectively and its inhibitory site in M. aeruginosa is located in PSII. The target M. aeruginosa and non-target C. pyrenoidosa showed totally different tolerance to berberine. The difference in the photosystem structures of these two algae might be responsible for their different sensitivities to berberine. It is reasonable to predict that the selective algicidal activity of berberine would lead to the replacement of susceptible target M. aeruginosa by tolerant non-target C. pyrenoidosa.

This work was financially supported by the Natural Science Foundation Grant of Tianjin (Grant Nos. 16JCYBJC29900, 17JCYBJC29500 and 18JCZDJC7800), the National Natural Science Foundation of China (Grant No. 31772857), the Modern Aqua-ecology and Health Aquaculture Innovation Team of Tianjin (Grant No. TD13-5089), Tianjin modern industrial technology system (Grant No. ITTFRS 2017015) and Tianjin Key Laboratory of Animal and Plant Resistance.

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Author notes

These authors contribute equally to this work.