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All issues Volume 54 (2018) Ann. Limnol. - Int. J. Lim., 54 (2018) 8 Full HTML
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Ann. Limnol. - Int. J. Lim.
Volume 54, 2018
Article Number 8
Number of page(s) 7
DOI https://doi.org/10.1051/limn/2018003
Published online 01 March 2018

© EDP Sciences, 2018

1 Introduction

Allelopathy, derived from the words ‘allelon’ and ‘pathos’, is a process by which specific biomolecules are secreted by one plant or bacterial species to possibly inhibit or benefit other plants or bacterial species. In aquatic ecosystems, allelopathic interaction also occurs between algae and plays an important role in species competition, succession except for other factors, such as hydrodynamics, nutrients and temperature (Suikkanen et al., 2004; Dunker et al., 2013; Rzymski et al., 2014; Accoroni et al., 2015; Wang et al., 2017b). Many examples of allelochemical interactions exist amongst cyanobacteria and their competitors which may affect the seasonal dynamics of these algae (Legrand et al., 2003). For example, allelochemicals secreted by Cylindrospermopsis raciborskii can inhibit the growth of its competitors, such as Microcystis aeruginosa, thereby contributing to the stable dominance of C. raciborskii in a tropical lake (Figueredo et al., 2007; Mello et al., 2012). In Lake Kinneret, high biomass of Microcystis are observed until the end of winter, thereby causing either missing or delayed Peridinium bloom (Sukenik and Kaplan, 2002; Vardi et al., 2002). Sukenik and Kaplan (2002) and Vardi et al. (2002) further suggested that the filtrate of Microcystis monoculture can significantly inhibit the growth of the dinoflagellate Peridinium gatunense. In addition, M. aeruginosa elicits allelopathic effects on competitive Scenedesmus quadricauda (Zheng et al., 2008) and Quadrigula chodatii (Zhang et al., 2013). Cyanobacteria and green algae also demonstrated seasonal changes in eutrophic lakes, such as Lake Taihu (Cai et al., 2012) and Lake Dianchi (Dong et al., 2015) in China. Bar-Yosef et al. (2010) also demonstrated that the monoculture of Aphanizomenon ovalisporum can secrete allelochemicals on competitors. The underlying mechanism may involve the promotion of phosphorus (Pi) supply by cylindrospermopsin producers through the induction of alkaline phosphatase secretion in other phytoplankton, suggesting that their abundance increases despite the reduced (Pi) supply from watersheds (Bar-Yosef et al., 2010).

Growth effects have been extensively investigated. In fact, the interaction between algae can induce growth effects but also have morphological influences (Mello et al., 2012). These morphological influences might also be essential for algal competition and interaction. However, studies on morphological influences amongst phytoplankton have been rarely performed. During growth, which is related to the beginning and the full Microcystis dominance/bloom in nature, substances produced in different growth phases are diverse. Studies comparing the effects of extracellular metabolites from different growth phases are also limited.

We hypothesised that morphological responses could be detected between algal interactions, in addition to growth effects. Furthermore, we assumed that the morphological and growth responses of other algae to M. aeruginosa were growth-phase dependent. To test this hypothesis, we chose a toxic cyanobacterium, namely, M. aeruginosa, and two common green algae, namely, Chlorella vulgaris and Kirchneriella sp., as target species. This study aimed to demonstrate (1) the growth responses of two green algal strains to M. aeruginosa; (2) whether M. aeruginosa influences the morphological characteristics of two green algal strains; (3) whether filtrates of M. aeruginosa from different cultivation phases have various influences on the growth and morphological characteristics of the target green algae. This study contributed new insights into the allelopathic interaction between algae and provided a new theoretical basis for algal succession in eutrophic lakes, rivers, reservoirs and aquaculture ponds.

2 Materials and methods

2.1 Algal culture

Axenic strains of toxic cyanobacteria M. aeruginosa (FACHB-905) and green alga C. vulgaris (FACHB-8) and Kirchneriella sp. (FACHB-1134) were all obtained from Freshwater Algal culture Collection of Institute of Hydrobiology, Chinese Academy of Sciences (deposited in Wuhan, China). M. aeruginosa (FACHB-905) was isolated from Dianchi Lake (Kunming, China), and was reported to produce microcystin-LR at approximately 0.61 µg per 107 viable cells (Sun et al., 2012).

Prior to the experiment, all strains were cultured separately with sterile BG11 medium (Rippka et al., 1979), at a climate-controlled temperature of 25 °C, under a cool-white fluorescent illumination of 25 μmol photons s−1 m−2 in a 12 h:12 h light–dark cycle. Both cultures were shaken three times per day to prevent sedimentation.

2.2 Experimental design

2.2.1 Preparation of cell-free filtrates associated with M. aeruginosa

The biomass of M. aeruginosa was determined by its optical density (OD) at 665 nm (blue-green algae) under ultraviolet/visible spectrophotometer, and the initial OD665 was 0.2 (with cell density 1.86 × 109 cells/L). The incubation conditions were the same as the maintenance of stock cultures, as mentioned above.

One part of the cell-free M. aeruginosa filtrate was obtained when M. aeruginosa grew to the exponential phase (EP) (cultured for 5 days, when OD665 = 0.56) and the other part was harvested in the stationary phase (SP) by cultivating for 30 days (when OD665 = 1.56) after inoculation (Wang et al., 2017a). M. aeruginosa cultures of different growth phases were centrifuged with a speed of 8000 r m−1 for 10 min. Then, each supernatant was filtered through Whatman GF/C filters (Whatman International Ltd., Maidstone, England) for subsequent experimentation (Mello et al., 2012).

2.2.2 Effects of cell-free filtrates associated with M. aeruginosa on C. vulgaris and Kirchneriella sp.

When the two green algae were in the exponential stages, the formal experiment started. The experiment was performed in 250 mL Erlenmeyer flasks. The experiment had two treatments (EP, SP), in addition to the control, which had no Microcystis filtrate (filtrated BG11 medium). The initial inoculation at OD680 (OD at 680 nm for green algae) of the tested green alga C. vulgaris and Kirchneriella sp. was 0.1 for both, with cell densities of 4.57 × 108 cells/L and 3.98 × 108 cells/L, respectively. Each treatment was repeated in triplicate; thus, 18 culture flasks were obtained in total. Cells grew in flasks containing 150 mL of solution (controls, filtrate BG11 medium; in cell-free filtrates in EP or SP, nutrients were added similar to that of BG11 medium to compensate for nutrient decrease during the preliminary cultivation period) (Mello et al., 2012).

Each culture was cultivated in conditions similar to those described above and shaken three times daily to avoid sedimentation. The experiments lasted for 7 days, and each algal culture was sampled every day to measure growth, colony proportion and cell numbers per colony in C. vulgaris and Kirchneriella sp. The details were as follows: samples of 3 mL were used to determine the biomass of the target green algae C. vulgaris and Kirchneriella sp. by measuring its OD at 680 nm (OD680) (ultraviolet/visible spectrophotometer), and samples of 2 mL were fixed with Lugol’ solution and viewed under an inverted microscope within 24 h at 400× magnification to determine the cell density, colony proportion and number of cells per colony (Lürling and Van Donk, 1997). In the study, the colony was identified as a minimum of three cells; the colony proportion was determined using the ratio between the number of cells in colonies and the total number of algae counted in each treatment. The number of cells per colony was assessed by the ratio of the total number of algae counted and the number of colonies in each treatment.

2.3 Statistical analysis

The slope of the regression between ln-transformed OD680 and the experimental time (day) was used as an estimate of the population growth rate (Lürling, 2006; Mello et al., 2012). The effect of the growth phase of M. aeruginosa on the growth rate of target algae was tested using a one-way ANOVA with the growth phase as an independent factor and subsequent separate post hoc tests to detect the differences between treatments (α = 0.05) (Fisher LSD) (Wang et al., 2017a).

The percentage of the cells in the colonies and the number of cells per colony of each treatment during the experiment were compared through a repeated-measure ANOVA (α = 0.05). Both tests were followed by Tukey’s post hoc tests to detect the differences between treatments (α = 0.05). P < 0.05 was considered significant in all of the analyses. Mauchly’s sphericity was examined, and data were log-transformed when necessary. These tests were performed in SPSS 13.0 for Windows.

3 Results

3.1 Growth effects of M. aeruginosa filtrates on C. vulgaris and Kirchneriella sp.

The growth of C. vulgaris was slightly reduced on day 2, compared with that of the control (Fig. 1a). At the end of the experiment, we determined the growth rate of C. vulgaris and found that M. aeruginosa filtrate in EP and SP significantly increased the growth of C. vulgaris (F = 21.856, P = 0.002); however, further post hoc tests indicated that no significant differences were detected in growth rates of C. vulgaris in the treatment with M. aeruginosa filtrate in EP and SP (P = 0.672) (Fig. 1b).

The growth rates of Kirchneriella sp. in the treatment with M. aeruginosa filtrate in EP and SP were also significantly influenced compared with those of the control (F = 65.805, P = 0.000). Furthermore, post hoc tests showed that the growth of Kirchneriella sp. was significantly decreased when it was treated with M. aeruginosa filtrates under EP (P = 0.001), but was increased significantly when it was treated with M. aeruginosa filtrates under SP (P = 0.001) (Fig. 2).

thumbnail Fig. 1

OD680 (a) and growth rate (b) of C. vulgaris in the control and treatment with filtrate of M. aeruginosa.
thumbnail Fig. 2

OD680 (a) and growth rate (b) of Kirchneriella sp. in the control and treatment with filtrate of M. aeruginosa.

3.2 Effects of M. aeruginosa filtrates on the morphological characteristics of two green algae

In addition to growth effects, the colony formation of C. vulgaris could be stimulated and its colony proportion could be significantly increased by M. aeruginosa filtrates (Fig. 3). The largest colony formed on day 2, and the number of cells per colony gradually decreased and reached values similar to that of the control at the end of the experiment.

According to repeated-measure ANOVA, the morphological response of C. vulgaris to M. aeruginosa filtrates was significantly influenced by the phase of M. aeruginosa filtrate treatment. The day and interaction between day and phase also significantly affected the number of cells per colony (day effects: F = 161.728, P = 0.000; treatment effects: F = 3138.241, P = 0.000; day × treatment effects: F = 72.352, P = 0.000) and colony proportion of C. vulgaris (day effects: F = 29.213, P = 0.000; treatment effects: F = 1094.324, P = 0.000; day × treatment effects: F = 9.713, P = 0.000). Tukey’s post hoc test indicated that M. aeruginosa filtrates in EP and SP significantly increased the number of cells per colony in C. vulgaris (P = 0.000) compared with those in the control. The effects of M. aeruginosa filtrate in SP on the increase in the number of cells per colony of C. vulgaris were stronger than those in EP (P = 0.000). According to Tukey’s post hoc test, the colony proportion of C. vulgaris in the control w C. vulgaris as significantly lower than that of M. aeruginosa filtrate treatment in EP and SP (P = 0.000). The colony proportion of C. vulgaris in SP was much higher than that of C. vulgaris in EP (P = 0.003).

The treatment with M. aeruginosa filtrate at different cultivation phases also significantly influenced the cell number per colony (repeated ANOVA, day effects: F = 13.242, P = 0.000; treatment effects: F = 211.252, P = 0.000; day × treatment effects: F = 6.589, P = 0.000) and colony proportion (repeated ANOVA, day effects: F = 92.966, P = 0.000; treatment effects: F = 590.400, P = 0.000; day × treatment effects: F = 23.268, P = 0.000) of Kirchneriella sp (Fig. 4) . Furthermore, Tukey’s post hoc test indicated that significant differences were detected in the number of cells per colony of Kirchneriella sp. between the control and M. aeruginosa filtrates in EP and SP (P = 0.000). According to Tukey’s post hoc test, the colony proportion of Kirchneriella sp. in the control was significantly lower than that in M. aeruginosa filtrate treatment in EP (P = 0.001). The colony proportion of Kirchneriella sp. in SP was much lower than that in M. aeruginosa filtrate in EP (P = 0.000).

thumbnail Fig. 3

Cell number per colony (a) and colony proportion of C. vulgaris (b), in the control and treatment with filtrate of M. aeruginosa.
thumbnail Fig. 4

Cell number per colony and colony proportion of Kirchneriella sp. (b) in the control and M. aeruginosa filtrate.

4 Discussion

Culture filtrate method is a classic approach to determine allelopathy between phytoplankton species (Wang et al., 2017b). Considering our hypothesis, we demonstrated the remarkable allelopathic effects of toxic M. aeruginosa on C. vulgaris and Kirchneriella sp. Our results also suggested that M. aeruginosa filtrate could cause growth effects (growth rate) and influence the morphological characteristics of the tested green algae. To the best of our knowledge, this study is the first to report the cyanobacterium-induced colony formation of green algal strains. Moreover, our studies suggested that these effects were dependent on the growth stages of M. aeruginosa and the strain of the target algae.

Allelopathy functions through the release of allelochemicals into the surrounding water which can negatively affect other competitive organisms. However, allelopathic stimulations have been also reported in the interaction between algae (Pratt, 1966; DellaGreca et al., 2010; Campos et al., 2013). Our results also indicated that M. aeruginosa filtrates could promote the growth rate of C. vulgaris. This consistency might be attributed to the dependence of the effects of algae on their concentration (Campos et al., 2013; Pinheiro et al., 2013; Rzymski et al., 2014; B-Béres et al., 2015). Pratt (1966) suggested that high concentrations of Olisthodiscus luteus can inhibit the growth of Skeletonema costatum, whereas low concentrations stimulate the growth of S. costatum. DellaGreca et al. (2010) further reported that the growth of Pseudokirchneriella subcapitata is stimulated by C. vulgaris of low densities but is inhibited by C. vulgaris of high densities. Low concentrations of cyanobacteria or crude extracts can promote the growth of C. vulgaris (Campos et al., 2013), Chlamydomonas reinhardtii and Nannochloropsis sp. (Pinheiro et al., 2013). Song et al. (2013) also indicated that the growth of Botryococcus braunii is induced by filtrates derived from low or moderate C. vulgaris density cultures but is prevented in the filtrate derived from a high C. vulgaris density culture. The present study also discussed the influences of the cultivation phase of M. aeruginosa filtrate on the target algae. Some studies reported that the inhibitory effects of filtrates in SP are stronger than those of other growth phases (Arzul et al., 1999; Suikkanen et al., 2004; Wang et al., 2017b). Conversely, other studies have indicated that the effects of filtrates obtained from cultures of SP on target species are weaker than those derived from the same monoculture in EP (Suikkanen et al., 2004; Zhang et al., 2013; Wang et al., 2017a). The present study revealed that the effects of different cultivation phases of M. aeruginosa on target algae were also species dependent (Leflaive and Ten-Hage, 2007). For C. vulgaris, no significant differences were detected in the growth effects caused by M. aeruginosa filtrate in EP and SP. However, M. aeruginosa filtrate in EP inhibited the growth of Kirchneriella sp., whereas M. aeruginosa filtrate in SP significantly promoted its growth.

Many studies about phytoplankton phenotypic plasticity induced by physio-chemical variables, zooplankton, submerged plants or other algae have been published (Mulderij et al., 2005; Leflaive et al., 2008; Van Donk et al., 2011; Mello et al., 2012; Dong et al., 2013, 2018). In addition to growth effects, the morphological responses of the two green algae to M. aeruginosa filtrate were described, and such responses were dependent on cultivation phase. For C. vulgaris, M. aeruginosa filtrate treatment promoted algal cells (C. vulgaris) to aggregate into more colonies compared with that of the control, and the effects of the SP filtrate were stronger than those of the EP filtrate. In our study, despite the slight inhibition of the growth of C. vulgaris at the beginning of the experiments, the final growth rate of C. vulgaris was enhanced. One explanation for this might be that the initial growth inhibition was related to the colony formation, that the growth inhibition was similar to the peak of colony formation of C. vulgaris. In the present study, the fresh cell-free M. aeruginosa filtrate was only added once at the beginning of the experiment (the concentration was maximal) and showed strong effects on colony formation of the target algae in the beginning. Thereafter, the colonies gradually broke into small colonies and single cells; until the end of the experiment (the seventh day), no differences were detected between control and filtrate treatment. This might be due to the degradation of the allelochemicals with the increasing experimental time. At the beginning of the experiment, the high amount of allelochemicals promoted the colony formation of the target algae, the process of which needed excessive investment of energy to accumulate more intracellular carbohydrate, which inhibited the growth of target algae Scenedesmus (Zhu et al., 2016). Whereas, Dong et al. (2018) suggested that with the degradation of active compounds of the filtrate, the carbohydrates stored in colonies might provide sufficient energy for target algae C. vulgaris to grow and develop. Thus, in a laboratory experiment, the one-time addition of filtrates might be advantageous for the growth of C. vulgaris.

The response of growth and morphology of Kirchneriella sp. was different from that of C. vulgaris. The present results suggested that filtrates of M. aeruginosa in EP significantly promoted big and numerous colonies in Kirchneriella sp. These colonies still existed until the end of the experiments. Filtrates of M. aeruginosa in SP were accompanied with a small cell colony of Kirchneriella sp. This result was also considered to provide a theoretical basis for the different responses of Kirchneriella sp. to filtrates of M. aeruginosa in various cultivation phases. Colony formation required high amounts of energy, thus inhibiting growth, whereas single cells were preferable for algal growth (Zhu et al., 2016). The different morphological responses of Kirchneriella sp. to filtrates of M. aeruginosa in EP and SP suggested that the two phases might possess various active ingredients which should be further identified and analysed (Pakdel et al., 2013). Besides, the different responses of C. vulgaris and Kirchneriella sp. also suggested that the allelochemicals effects were species-dependent.

Finally, we discussed the substances implicated in the interaction between algae. Different allelochemical substances, including amino acids, enzymes, lipids, vitamins and toxins, released during algal growth might affect the growth of other algae (Leflaive and Ten-Hage, 2007). The secretion of exopolysaccharide (EPS) promotes the colony formation of target algae (Yang et al., 2009; Yang and Kong, 2012). In our tests involving M. aeruginosa filtrates, a high amount of EPS was detected compared with that of the control (data not shown here). Thus, EPS might influence our study on algal colony formation, and other substances were implicated in this process. A large colony was detected in Kirchneriella sp. under EP M. aeruginosa filtrate treatment, whereas a small colony was observed in SP treatment compared with those of the control. For Microcystis, microcystin (MC) was considered a key factor affecting other algae (Valdor and Aboal, 2007; Yang et al., 2014), and several cases involving MCs as allelopathic compounds have been reported (Pflugmacher, 2002; Yang et al., 2014; Bittencourt-Oliveira et al., 2015). The allelochemical properties of MC have been debated (Babica et al., 2006), and recent reports have revealed that a non-toxic Microcystis strain can affect the growth of C. vulgaris (Ma et al., 2015). Thus, other allelochemicals should be discussed in future studies.

Acknowledgement

This work was supported by the National Nature Science Foundation Project of China (NO. 31500380) and Dr. Start-up Foundation Project of Henan Normal University (NO. qd14183) and the Key Scientific and Technological Project of Henan Province (NO. 152102310314 & 172102210352).

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Cite this article as: Dong J, Chang M, Li C, Li J, Shang X. 2018. Morphological and growth responses of two green algal strains to toxic Microcystis are dependent on the cultivation growth phase of filtrate and target strain. Ann. Limnol. - Int. J. Lim. 54: 8

All Figures

thumbnail Fig. 1

OD680 (a) and growth rate (b) of C. vulgaris in the control and treatment with filtrate of M. aeruginosa.
In the text
thumbnail Fig. 2

OD680 (a) and growth rate (b) of Kirchneriella sp. in the control and treatment with filtrate of M. aeruginosa.
In the text
thumbnail Fig. 3

Cell number per colony (a) and colony proportion of C. vulgaris (b), in the control and treatment with filtrate of M. aeruginosa.
In the text
thumbnail Fig. 4

Cell number per colony and colony proportion of Kirchneriella sp. (b) in the control and M. aeruginosa filtrate.
In the text

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