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All issues Volume 58 (2022) Int. J. Lim., 58 (2022) 4 Full HTML
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Int. J. Lim.
Volume 58, 2022
Article Number 4
Number of page(s) 9
DOI https://doi.org/10.1051/limn/2022004
Published online 25 May 2022

© EDP Sciences, 2022

1 Introduction

Globally distributed freshwater green algae are not defenseless but instead possess the characteristic of phenotypic plasticity. That is, one genotype can exhibit a variety of phenotypes under different environmental conditions. Among morphological responses, colony formation is one of the most common strategies utilized by green algae to address adverse environmental pressures (Tukaj and Bohdanowicz, 1995; Lürling and Beekman, 2002; Lürling, 2006; Li et al., 2013; Fisher et al., 2016; Huang et al., 2016; Pan et al., 2017; Dong et al., 2018; Herron et al., 2019; Sun et al., 2020; Wan et al., 2020; Cheloni and Slaveykova, 2021). Numerous studies have indicated that colonial cells show considerably higher resistance to global warming, UVB irradiation, high salt, and micropollutants than single cells (Tukaj and Bohdanowicz, 1995; Khona et al., 2016; Huang et al., 2018; Li et al., 2018; Zhu et al., 2019; Cheloni and Slaveykova, 2021).

Colony formation by green algae under induction by interspecific infochemicals has received great attention in recent decades. Hessen and van Donk (1993) reported that the filtrate of Daphina magna could induce the colony formation of Desmodesmus subspicatus. Green algae have been suggested to be capable of transforming into eight-cell colonies within 3–5 days. Thus far, numerous studies have demonstrated the induced colony aggregation in Scenedesmus by Brachionus calyciflorus (Yang et al., 2006), Scenedesmus by Daphnia (Lürling and van Donk, 2000; van Holthoon et al., 2003; Verschoor et al. 2004; Yang and Li, 2007; Zhu et al., 2017), Chlorella vulgaris by Ochromonas vallescia (Boraas et al., 1998), C. vulgaris by Tetrahymena thermophila (Fisher et al., 2016), Chlamydomonas reinhardtii by B. calyciflorus (Lürling and Beekman, 2006), and C. reinhardtii by Paramecium tetraurelia (Herron et al., 2019). Induced colony formation could increase the size and prevent the predation of small herbivorous zooplankton, as well as increase the anti-predation capability of green algae (Van Donk et al., 2011; Pančić and Kiørboe, 2018; Lürling 2021), thus influencing the energy flow of food webs (Wan et al., 2020). Given this fact, phytoplankton morphology is another potential important factor involved in shaping phytoplankton structure and food webs. Pollution caused by human activities has been recently suggested to be capable of interrupting colony formation by herbivorous zooplankton under infochemical induction. Huang et al. (2016) performed an indoor simulation experiment and suggested that low concentrations of free Cu2+ had no significant effects on algal growth and photosynthesis but had the capability to inhibit S. obliquus colony formation in response to Daphnia filtrate. Pan et al. (2017) indicated that norfloxacin could also disrupt Daphnia magna-induced colony formation. Zhu et al. (2019) demonstrated that colony formation by Daphnia was inhibited even by low Zn2+ concentrations, and colony size decreased as the Zn2+ concentration was increased. Sun et al. (2020) revealed that elevated UVB not only reduced the growth of S. obliquus but also disturbed its Daphnia-induced colony formation, thus increasing its vulnerability to predation and likely leading to potential shifts in plankton food webs.

In addition to colony formation under the influence of infochemicals from herbivorous zooplankton, the effects of submerged macrophytes on the morphology of green algae have been emphasized recently. The macrophyte-induced colony formation of green algae was first reported by Mulderij et al. (2005), who demonstrated that Stratiotes aloides induced colony formation of S. obliquus. Subsequently, in our previous studies, we demonstrated that colony formation of S. obliquus was induced by Ceratophyllum demersum (Dong et al., 2013) and that C. vulgaris was induced by C. demersum (Dong et al., 2018, 2019) and Potamogetom crispus (Chang et al., 2020). Similar to previous studies, we also suggested that the increased exopolysaccharide secretion of the target algae might be responsible for this colony formation (Dong et al., 2018; Khona et al., 2016). A recent study by Sun et al. (2020) also demonstrated that the carbohydrate-regulated gene expression was related to the colony formation of S. obliquus. However, to the best of our knowledge, little is known about how environmental pressure affects this colony formation of green algae by submerged macrophytes. Nowadays, most freshwater ecosystems worldwide are suffering from eutrophication. Microcystis, one of the major players in toxic cyanobacterial blooms, can produce secondary metabolites, such as microcystins, which are cyclic heptapeptide compounds with hepatotoxic effects on humans (Chen et al., 2009) and wild life (Wang et al., 2021). In field ecosystems, microcystins are mainly retained within cyanobacterial cells but are released into the water after cell lysis during the collapse of heavy blooms; microcystin concentrations could thus reach very high levels (Yang et al., 2011). Among the various isomers of microcystins, microcystin LR (MC-LR) has the strongest toxicity and is the most widely distributed (Omidi et al., 2018; Pham and Utsumi, 2018). Thus far, whether the microcystins secreted by Microcystis could influence the morphology of green algae has rarely been discussed. To our knowledge, little is known about the effects of microcystins on the colony formation of green algae induced by submerged macrophytes.

C. vulgaris is an asexual freshwater green alga that is found worldwide and that usually lives in unicellular populations. P. crispus is also commonly found in eutrophic freshwater habitats. On the basis of the information presented above, in this work, we (1) simulated the morphological responses of the green alga C. vulgaris to MC-LR; (2) detected the effects of filtered extracts and exudates from the submerged macrophyte P. crispus on C. vulgaris; and (3) discussed the possible effects on P. crispus–C. vulgaris systems contaminated by MC-LR. This study provides a theoretical basis for understanding the roles of secondary metabolites in the phenotypic plasticity of green algae and the interaction between infochemicals from green algae and macrophytes in cyanotoxin-contaminated ecosystems. Our study will provide more insights for the cyanobacterial blooms ecosystems restoration by submerged macrophytes.

2 Materials and methods

2.1 Algal culture

The green algal strain (C. vulgaris) was obtained from the Freshwater Algae Culture Collection of the Institute of Hydrobiology (FACHB-8), Chinese Academy of Sciences, Wuhan, China. Prior to experimentation, stock cultures of C. vulgaris were established under favorable conditions at room temperature (25 °C) in 500 mL Erlenmeyer flasks with 300 mL of BG11 medium (Rippka et al., 1979) under a 12 h light:12 h dark cycle (25 μmol photons s−1 m−2). The cultures were shaken three times a day to prevent sedimentation, and the algae C. vulgaris were utilized for further experimentation when they grow to the exponential phase after 7 days acclimation.

2.2 Extract and exudate preparation of macrophytes

P. crispus samples were collected from Weihe River (35°18ʹ50.8ʹʹN, 113°54ʹ27ʹʹE) near Henan Normal University, China, and were carefully rinsed with tap water to remove all adhering epiphytes and zooplankton (Lürling et al., 2006). Subsequently, the macrophytes were acclimatized with C. vulgaris (1.1 × 109 cells L−1) for 3 days for the following experiments. The preliminary preparation and acclimation protocols were conducted as follows: 12 g of fresh weight of P. crispus was acclimatized with 1200 mL of C. vulgaris (initial density: 1.1 × 109 cells L−1) in BG11 medium for 3 days for the following experiments, thus the concentration of the macrophytes was 10 g L−1. Meanwhile, in the control group, 1200 mL of C. vulgaris (initial density: 1.1 × 109 cells L−1) was cultivated in BG11 medium for 3 days without any macrophytes. All the groups were set in climate-controlled temperature at 25 °C under a 12 h light:12 h dark cycle (25 µmol photons s−1 m−2).

Macrophyte exudates (1200 mL) were obtained from the acclimation medium of P. crispus with C. vulgaris. The acclimated P. crispus was carefully rinsed with sterile water and ground with 1200 mL of sterile water. Subsequently, 1200 mL of C. vulgaris in the control group, exudates, and extracts were centrifuged at 8000 r min−1 for 10 min. Then, all the supernatants were filtered with 0.22 μm filters for later use. Meanwhile, 1200 mL of BG11 medium was also prepared as the blank group to discard the influences of C. vulgaris.

2.3 Experimental design

Before the formal experimentation, 1200 mL of macrophyte exudates was divided into two parts. One part was added with MC-LR (30 μg L−1). Moreover, 1200 mL of macrophyte extracts, 1200 mL of C. vulgaris filtrates, and 1200 mL of BG11 medium were divided into two parts. One part was added with MC-LR (30 μg L−1). Eight groups were obtained: (1) 600 mL of BG11 medium; (2) 600 mL of BG11 medium with MC-LR; (3) 600 mL of C. vulgaris filtrates; (4) 600 mL of C. vulgaris filtrates with MC-LR; (5) 600 mL of macrophyte exudates; (6) 600 mL of macrophyte exudates with MC-LR; (7) 600 mL of macrophyte extracts; and (8) 600 mL of macrophytes extracts with MC-LR.

Subsequently, the target alga C. vulgaris was inoculated into all eight groups at the initial inoculation density of 1.1 × 109 cells L−1. Each group was supplemented with nutrients similar to those in BG11 medium to compensate for nutrient reduction during the preliminary cultivation period. Finally, each group was divided into three 250 mL Erlenmeyer flasks with 200 mL volumes as the three replicates; thus, 24 culture flasks were obtained in total. All the cultures were cultivated under favorable conditions as described above and shaken three times every day to avoid sedimentation. The experiments lasted for 9 days, and each algal culture was sampled twice a day for the measurements of the growth, colony proportion, and cell numbers per colony of C. vulgaris. MC-LR dynamics were also detected.

2.4 Parameter measurements

2.4.1 Algal density and morphology composition

Samples (2 mL) were fixed with Lugol’s fixative and viewed under an inverted microscope with 400× magnification to count cell density, cell number per colony, and colony proportion (minimum of three cells) (Lürling and Van Donk, 1997).

2.4.2 Growth rate of C. vulgaris

Growth rate (μ) was calculated by using the following equation: μ = (ln x2 − ln x1)/(t2 − t1), where x1 and x2 represent algal density at time t1 and t2, respectively.

2.4.3 Photosynthetic pigments

Samples (5 mL) were centrifuged at 12,000 r min−1 for 10 min. The centrifuged algal cells were extracted with 95% ethanol for 24 h at 4 °C in the dark (shaking extraction for approximately 12 h to extract pigments fully). Then, all the extracted substances were centrifuged, and 3 mL of supernatant was measured by using an ultraviolet/visible spectrophotometer. Absorbance was measured at 665, 649, and 470 nm (A665, A649, and A470), and photosynthetic pigment concentrations were calculated as follows (Lichtenthaler and Buschmann, 2001): Chl a (mg L-1)=13.95×A665−6.88×A649,(1) Ccaro=(1000×A470−2.05×Achla)/245.(2)

2.5 Statistical analysis

Mean values and standard deviations were calculated for different replicates (n = 3). One-way analysis of variance (ANOVA) with LSD post-hoc test was conducted by using SPSS 22.0 for Windows to compare significant differences between each treatment in the algal density, growth rate, photosynthetic pigments, colony percentage, and cell number per colony under each treatment (Wang et al., 2017). p < 0.05 was considered statistically significant in all of the analyses. Significance was marked with different alphabet when detected between two groups.

3 Results

3.1 Growth of C. vulgaris

During the first day of cultivation, which was considered as the lag period, C. vulgaris treated with the control and the exudates and extracts of P. crispus exhibited slow growth ( Figs. 1b and 1d). During the subsequent period, the presence of the macrophyte substances significantly inhibited the growth of C. vulgaris (p < 0.05). The inhibitory effects of the extracts were greater than those of the exudates (Figs. 1e and 1f). Furthermore, in contrast to our expectation, the addition of MC-LR had no significant influences on the growth of C. vulgaris and the inhibitory effects of P. crispus (p > 0.05).

thumbnail Fig. 1

Individual and combined effects of MC-LR with P. crispus (exudates or extracts) on the algal density and growth rate of C. vulgaris.

3.2 Photosynthetic pigments

Compared with those in the control treatment, Chl a and carotenoid contents were significantly reduced under treatment with the exudates and extracts of P. crispus (p < 0.05). As shown in Figures 2e and 2f, the inhibitory effect of the extracts on C. vulgaris was significantly more obvious than those of the exudates of P. crispus (p < 0.05). The inhibitory effects of the exudates were reduced on day 9 of the experiment. At this time, no significant differences were detected between the pigment contents under the control and exudate treatments (p > 0.05). However, in contrast to the exudates, the extracts of P. crispus exerted persistent inhibitory effects on the growth of C. vulgaris. The inhibitory effects of the extracts of P. crispus were still detected at the end of the experiment (Fig. 2).

At the experimental concentration used in this study, MC-LR had no significant effects on the photosynthetic pigments (Chla and carotenoids) of C. vulgaris (p > 0.05). The addition of MC-LR exhibited no significant influences on the inhibition ofC. vulgaris growth caused by the exudates and extracts ofP. crispus (p > 0.05).

thumbnail Fig. 2

Individual and combined effects of MC-LR with P. crispus (exudates or extracts) on the Chl a and carotenoid concentrations of C. vulgaris.

3.3 Algal morphology

As illustrated in Figure 3a, the average cell numbers per colony at most of the time points demonstrated no significant differences (except for those on day 3) (p > 0.05). However, 3 days after a short adaptation period, the exudates of P. crispus induced a significant increase in the colony counts of C. vulgaris in the control and treatment groups (p < 0.05). The percentage of algal colonies (>4 cells) under treatment with P. crispus exudates was significant and approximately 1.2% higher than that under the control during days 3–5 of the experiment (Fig. 3b). However, from day 7 of the experiment, the increased colonies decreased and gradually transformed into small colonies (<4 cells) or single cells (Fig. 2b). In addition, it was also demonstrated that the presence of MC-LR exerted no obvious effects on the morphology of C. vulgaris and the morphological changes induced by the exudates of P. crispus during the whole cultivation period (p > 0.05).

The morphological changes induced by P. crispus extracts were significantly bigger than those induced by the exudates (Figs. 3e and 3f) (p < 0.05). Cell number per colony and colony percentage increased within 24 h. However, as shown in Figures 3c and 3d, given that the induced effects were temporary, the induced colonies gradually shrank or transformed into single-cell colonies in the later cultivation period. Meanwhile, no significant influences were detected on the P. crispus-induced morphological changes of C. vulgaris by MC-LR (p > 0.05).

thumbnail Fig. 3

Individual and combined effects of MC-LR with P. crispus (exudates or extracts) on the algal morphology of C. vulgaris.

4 Discussion

4.1 Growth effects of macrophytes on green algae

In aquatic ecosystems, submerged macrophytes and phytoplankton are in fierce competition because they have similar demands for nutrition, light, and other resources (Amorim and Moura, 2020). Allelopathy is one of the most important strategies that are utilized to alleviate the competition between submerged macrophytes and phytoplankton (Amorim et al., 2019; Amorim and Moura, 2020). Numerous studies have indicated that submerged macrophytes can secrete active allelochemicals and exert profoundly negative effects on the growth and photosynthetic activities of cyanobacteria (Mohamed, 2017). However, the effects of submerged macrophytes on green algae are inconsistent (Pełechata and Pełechaty 2010; Santonja et al., 2018; Zhao et al., 2012). Some researchers have indicated that compared with cyanobacteria, green algae are less sensitive to the allelochemicals secreted by submerged macrophytes (Pakdel et al., 2013; Santonja et al., 2018) and that the allelopathic effects of submerged plants on algae depend on the initial biomass of the submerged plant and initial algal density (Körner and Nicklisch, 2002; Wu et al., 2007). Our result was in agreement with the results reported by Chen (1999), who indicated that the growth of S. obliquus was promoted by low concentrations (<4 g FW L−1) of C. demersum, whereas algal growth was inhibited by high concentrations (>4 g FW L−1). In the present study, the growth of C. vulgaris was significantly reduced under treatment with P. crispus at a concentration of 10 g FW L−1, and the extracts exerted stronger inhibitory effects on the growth of C. vulgaris than the exudates. Our research result was consistent with the findings of Wu et al. (2011), who also discovered that the growth of S. obliquus co-cultivated with C. demersum was inhibited. However, in contrast to our expectation, the addition of MC-LR did not affect the growth of C. vulgaris and did not influence the effects induced by P. crispus. This result was consistent with the results of Zhu et al. (2014), who demonstrated that the growth rate of Scenedesmus obliquus was unaffected by MC-LR contamination (50 μg L−1), as well as the findings of Perreault et al. (2011), who reported that the saxitoxins released by Cylindrospermopsis raciborskii had no toxic effects on C. reinhardtii.

4.2 Algal morphology

In recent decades, a growing number of studies have indicated that morphological transformation is more sensitive to environmental pressure than growth effects. The interspecific infochemical-induced colony formation of green algae has been extensively reported. Related studies mainly focused on three aspects: infochemicals from herbivorous zooplankton ((Hessen and van Donk, 1993; Boraas et al., 1998; Lürling and van Donk, 2000; van Holthoon et al., 2003; Verschoor et al. 2004; Lürling and Beekman, 2006; Yang et al., 2006; Yang and Li, 2007; Fisher et al., 2016; Zhu et al. 2017; Herron et al., 2019;), competitive algae (Leflaive et al., 2008; Dong et al., 2019), and macrophytes (Dong et al., 2013; Dong et al., 2018, 2019; Chang et al., 2020). However, thus far, proof explaining the mechanisms of induced colony formation remains insufficient. One recognized explanation is that the colony formation of the target algae involves two steps: (1) fast algal growth and reproduction and (2) cell aggregation (Bisova and Zachleder, 2014; Li et al., 2015). Any factor influencing these two steps could inhibit algal colony formation. Although previous studies have found that the formation of green algal colonies is significantly related to the increased secretion of extracellular (intracellular) polysaccharides (Dong et al., 2018), the existing molecular mechanism of the colony formation in green algae induced by infochemicals of submerged macrophyte has rarely been studied. By now, only one study by Roccuzzo et al. (2020) analyzed the metabolism-related mechanism of colony formation in S. obliquus mediated by infochemicals from zooplankton resorting to iTRAQ quantitative proteomics analysis. Exploring the mechanism how the colony formation in green algae is stimulated and regulated between cells colonies by infochemicals is of great significance for further understanding information flow in food webs. In addition, our present work suggested that the submerged macrophyte P. crispus could induce colony formation by C. vulgaris. The morphological changes induced by the extracts of P. crispus were more obvious than those induced by exudates. Interestingly, the induced colony proportions of C. vulgaris (1–6%) in the present study were lower than those in previous studies (30–40%) (Dong et al., 2013, 2018, 2019; Chang et al., 2020) likely because the inhibitory effects on the growth of C. vulgaris indirectly affected the aggregation of algal cells.

The disturbance of interspecific infochemical-induced colony formation by environmental changes caused by human activities has received increasing attention. As mentioned above, heavy metals, herbicides, and global changes could considerably impair the colony formation induced by filtrate from the zooplankton Daphnia (Huang et al., 2016; Pan et al., 2017; Zhu et al., 2019; Sun et al., 2020). However, the addition of MC-LR did not induce morphological changes and did not interrupt the P. crispus-induced colony formation of C. vulgaris in the present study. This result was inconsistent with the finding of Bittencourt-Oliveira et al. (2016), who speculated that biochemical MCs may participate in colony formation of C. vulgaris. MC-LR, as one of the secondary metabolites of Microcystis, could promote accumulation of the intracellular and extracellular polysaccharides in Scenedesmus. And the polysaccharide secretion was increased with MC-LR concentration (Mohamed, 2008). The increase in polysaccharides might enhance cell viscosity, thus promoting colony formation by the target algae (Yang et al., 2007, 2010; Li et al., 2013, 2015; Bisova and Zachleder, 2014; Khona et al., 2016; Dong et al., 2018). Accordingly, MC-LR may play roles in algal colony formation. However, in the present simulation tests, the absence of the significant effects of MC-LR on algal morphology might be due to the low increase in polysaccharide content, which did not reach the threshold of morphological transformation, referred as Zhu et al. (2014) who also indicated that MC-LR had no significant influences on S. obliquus colony formation induced by Daphnia filtrate. Similar result by our previous study also found that MC-LR might not be responsible for the induced colony formation of C. vulgaris by M. aeruginosa (Dong et al., 2019). One explanation for this result could be attributed to the action of the two kinds of active substances; specifically, the infochemicals induced colony formation, whereas microcystin exerted no interaction effects, referred as Zhu et al. (2014). Notably, the performance of commercial MC-LR might be different from that of microcystin that naturally occurs in aquatic ecosystems. Therefore, in future studies, MCs secretion by Microcystis should be simulated, and their effects on morphological changes should be tested comprehensively.

Declaration of competing interest

The authors declare no conflicts of interest.

Acknowledgements

This work was financially supported by Young Backbone Teachers Project of Henan Province (No. 2020GGJS064), National Natural Science Foundation of China (No. 31500380), Scientific Fund of Henan Normal University (No. 2020QK02) and the Major public welfare projects in Henan Province (201300311300).

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Cite this article as: Dai D, Yang Y, Wang F, Zhang M, Gao Y, Dong J, Li X, Lv J. 2022. Effects of microcystin-LR on the colony formation of Chlorella vulgaris induced by the submerged macrophyte Potamogetom crispus. Int. J. Lim. 58: 4

All Figures

thumbnail Fig. 1

Individual and combined effects of MC-LR with P. crispus (exudates or extracts) on the algal density and growth rate of C. vulgaris.
In the text
thumbnail Fig. 2

Individual and combined effects of MC-LR with P. crispus (exudates or extracts) on the Chl a and carotenoid concentrations of C. vulgaris.
In the text
thumbnail Fig. 3

Individual and combined effects of MC-LR with P. crispus (exudates or extracts) on the algal morphology of C. vulgaris.
In the text

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