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All issues No 421 (2020) Knowl. Manag. Aquat. Ecosyst., 421 (2020) 36 Full HTML
Open Access
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 421, 2020
Article Number 36
Number of page(s) 8
DOI https://doi.org/10.1051/kmae/2020023
Published online 03 August 2020

© L. Lei et al., Published by EDP Sciences 2020

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

Toxic cyanobacterial blooms have widely occurred in freshwater ecosystems around the world, and are being facilitated by global warming (Paerl and Huisman, 2008; El-Shehawy et al., 2012). Bloom-forming cyanobacteria often cause severe problems in the management of water quality due to the release of cyanotoxins (Paerl et al., 2016). Microcystis is one of the most notorious genus which causes heavy blooms. Many Microcystis strains can produce hepatotoxin microcystins (MCs), and thus their bloom occurrence presents a risk to those who use blooming water for drinking, aquaculture, recreation and agricultural irrigation (Harke et al., 2016; Paerl et al., 2016). Numerous studies including both field investigations and laboratory experiments have been conducted to clarify the potential environmental drivers for the competitive advantages of Microcystis (Paerl and Huisman, 2008; El-Shehawy et al., 2012; Harke et al., 2016). The increasing temperature related to global warming is expected to promote its proliferation and dominance.

Previous studies showed that Microcystis strains exhibit a large degree of morphological, genetic and chemical diversity (Welker et al., 2004; Haande et al., 2007; Shen et al., 2007). Moreover, a high variability of growth and toxicity has been observed among strains of Microcystis (Vézie et al., 2002; Wilson et al., 2006; Xiao et al., 2017a), indicating each strain represent an ecotype able to adapt and to survive in changing environmental conditions (Pimentel and Giani, 2014). The recent comparative proteomic and genomic studies with different Microcystis strains have revealed a significant proportion of the identified proteins and that 127 to 911 genes were strain-specific (Alexova et al., 2011; Yang et al., 2015). These unique proteins or genes are assumed to be beneficial for survival and proliferation of Microcystis. Due to the existence of a high diversity at the inter-strain level, it is meaningful to investigate multiple Microcystis strains to explore the mechanism underlying their competitive advantage. Many previous laboratory studies usually used only one cyanobacterial strain to perform physiological experiments (Wu et al., 2009; Krüger et al., 2012), which are not adequate for our understanding of the effects of morphological, genetic or chemical variation among strains on cyanobacterial dynamics (Wilson et al., 2006; Shen et al., 2007; Willis et al., 2016).

Filamentous Raphidiopsis raciborskii (previously Cylindrospermopsis raciborskii) is another most successful bloom-forming cyanobacterial species in freshwater ecosystems. Studies of R. raciborskii explosively increased in the last decade due to its expansion into temperate region and its toxin-producing potential (Antunes et al., 2015; Burford et al., 2016). In some subtropical and tropical water bodies, co-existence or seasonal succession of M. aeruginosa and R. raciborskii is commonly observed (Costa et al., 2006; Moustaka-Gouni et al., 2007; Soares et al., 2009; Miller and McMahon, 2011). Changes in their relative dominance have been related to environmental and ecological conditions such as nutrient levels, physical factors, selective grazing and allelopathy (Moustaka-Gouni et al., 2007; Soares et al., 2009; Marinho et al., 2013; Rzymski et al., 2014). Due to this complicated scenario, predicting competition between M. aeruginosa and R. raciborskii is rather difficult.

Competition is a major factor shaping the phytoplankton structure and succession. Several studies investigated the effects of a variety of factors such as temperature, light, pH, nutrients and secondary metabolites on the growth and competition between M. aeruginosa and R. raciborskii (Figueredo et al., 2007; Mello et al., 2012; Marinho et al., 2013; Chislock et al., 2014; Rzymski et al., 2014; Thomas and Litchman, 2016; Xiao et al., 2017b; da Silva Brito et al., 2018). However, it has been realized that the effects of these factors remain inconsistent. For example, the relative and absolute biomass of M. aeruginosa declined and R. raciborskii was found to dominate in all N:P (from 7:1 to 122:1) treatments (Chislock et al., 2014), whereas R. raciborskii can either exclude or be displaced by M. aeruginosa under phosphorus limitation of 4.5 µmol L−1 K2HPO4 (Marinho et al., 2013). The morphological, genetic and chemical differences between strains of one species may contribute to the inconsistence (Marinho et al., 2013; Xiao et al., 2017b).

Temperature is among the major determinants which influence phytoplankton growth, nutrient uptake, and spatial-temporal distribution in freshwater systems. Both M. aeruginosa and R. raciborskii benefit from higher temperatures, which can give the two species a competitive advantage to outcompete other phytoplankton taxa through increased growth rates (Paerl and Huisman, 2008; O'Neil et al., 2012). As a tropical and invasive species, R. raciborskii seems to be one of the most likely cyanobacteria to benefit from global warming (Antunes et al., 2015). The persistent dominance of R. raciborskii has been observed in some tropical reservoirs, where M. aeruginosa occurred during a certain period (Branco and Senna, 1994; Figueredo and Giani, 2009; Soares et al., 2009; Jovanović et al., 2017). A recent study with monocultures reported that R. raciborskii strains had higher growth rates than toxic M. aeruginosa strains under a temperature above 20 °C, but had no apparent advantage over the non-toxic M. aeruginosa from 15 °C to 40 °C (Thomas and Litchman, 2016).

Accordingly, we hypothesize that both temperatures and strain differences may be crucial to for competition between M. aeruginosa and R. raciborskii. Currently, there are few studies assessing the effects of temperature on the competition of two species, and variation in stain-specific response has often been ignored. In this study, we examined competition between three strains of M. aeruginosa and one strain of R. raciborskii when exposed to different temperatures. We also tried to clarify the competitive abilities of M. aeruginosa with respect to the role of MC production.

2 Materials and methods

2.1 Strains and culture conditions

Two MC-producing M. aeruginosa strains FACHB905 and FACHB915, one non-MC-producing M. aeruginosa strain FACHB469 were provided by the culture collection of Chinese Academy of Science in Wuhan. R. raciborskii N8 was isolated from Zhenhai Reservoir, Guangdong Province, tropical China. All four strains were non-axenic. M. aeruginosa grew as single-cell populations and R. raciborskii filaments were straight. A pre-culture of each strain was grown at 25 °C in a 1 L Pyrex Erlenmeyer flasks containing 500 mL BG11 medium with an adjusted pH of 8.2 (Ripka et al., 1979). Erlenmeyer flasks were placed in a culture chamber with 30 µmol m−2 s−1 light intensity using cool white fluorescent lights. A 12/12 h light/dark cycle was systematically applied.

2.2 Competition experiments

In the pre-experiments, M.aeruginosa FACHB905 and R. raciborskii N8 were inoculated with different biovolume ratios (1:90, 1:180, 1:270, 1:450, 1:900 and 1:1800) to give R. raciborskii an initial advantage, however, we finally found M. aeruginosa FACHB905 exerted an exclusive competitive advantage and outcompeted R. raciborskii in all the competition experiments, regardless of the initial biovolume ratios (Fig. S1). Therefore, a lower biovolume ratio of 1:30 was applied throughout the competition experiments. Two-week-old cultures (in the exponential growth phase) served as inoculums. The inoculating cell densities of M. aeruginosa FACHB905, FACHB915 or FACHB469 and R. raciborskii N8 were 0.5 × 105 cell mL−1 and 0.5 × 105 filament mL−1, respectively, referred to as 1:30 biovolume ratio. The final volume of mixed cultures was 400 mL and each treatment was run in triplicate. The competition experiment was conducted under three temperature levels (LT = 16 °C, MT = 24 °C, HT = 32 °C). The flasks were gently mixed twice daily and samples of 2 mL were taken every 3−4 days for cell number counting. Cell numbers were counted in a Sedgewick Rafter counting chamber under an Olympus microscope with non-inverted optics at 400× magnification. The average cell size of a specie was obtained from the median volume of at least 100 random selected individuals according to the biovolume calculation methods by Hillebrand et al. (1999). Cell abundance of each species is converted to algal biovolume based on the average cell size of the species.

2.3 Effects of MC-LR on R. raciborskii N8

An experiment was designed to assess whether MC-LR or other allelopathic chemicals may be responsible for the competition ability of M. aeruginosa FACHB905. R. raciborskii N8 was harvested at the exponential growth phase and inoculated with initial chlorophyll-a concentration of 20 µg L−1 in 50 mL capped test tubes (25 mm × 150 mm) containing 35 mL of BG11 medium. The purified MC-LR (Alexis Biochemicals, USA) was added to each test tube and the final toxin concentration was as follows: 0, 0.1, 0.5, 1.0, 5.0, 10, 50, 100, 500 and 1000 µg L−1. Each treatment was carried out in triplicate and gently mixed twice daily. Chlorophyll-a (chla) concentrations were measured daily with aTD-700 laboratory Fluorometer (Turner Designs, California, USA). Significant difference (P < 0.05) among different treatments was tested by One-way ANOVA and Turkey's test in SPSS 16.0 statistical package.

2.4 Effects of spent medium of M. aeruginosa FACHB905 on R. raciborskii N8

In this experiment, spent medium of M. aeruginosa FACHB905 grown for 3 weeks was collected by separation of cells and medium via centrifugation. Subsequently, the supernatant was filter-sterilized through the injection filter with a nominal pore size of 0.22 µm (MILLEX-GP, Millipore, USA). Spent medium was then added to fresh BG11 medium with different volume ratios: 0%, 2.5%, 5.0%, 10%, 20%, 30%, 40% and 50%. R. raciborskii N8 was harvested and inoculated to the modified BG11 media as described in the first experiment. Each treatment was carried out in triplicate and gently mixed twice daily. Chlorophyll-a concentrations were measured daily with aTD-700 laboratory Fluorometer (Turner Designs, California, USA). The statistical analyses as showed in 2.3 were applied.

2.5 Effects of crude extract of M. aeruginosa FACHB905 on R. raciborskii N8

In this experiment, for the preparation of crude extract, 250 mL M. aeruginosa FACHB905 grown for 3 weeks was harvested by centrifugation, and the cell pellet was rinsed with sterile distilled water for three times. The resuspended cells were disrupted by freeze-thaw cycles and then 2 min sonication on ice. The suspension was centrifuged and the supernatant was filter-sterilized before added to fresh BG11 medium with different volume ratios: 0%, 0.33%, 0.67%, 1.67%, 3.33%, and 6.67%. R. raciborskii N8 was inoculated to the modified BG11 media as described in the first experiment. Each treatment was carried out in triplicate and gently mixed twice daily. Chlorophyll-a concentrations were measured daily with a TD-700 laboratory Fluorometer (Turner Designs, California, USA). The statistical analyses as showed in 2.3 were applied.

3 Results

3.1 Growth and competition of M. aeruginosa and R. raciborskii under three temperature levels

In the competition between 905 and N8 under three temperatures, M. aeruginosa completely displaced R. raciborskii, however, the competitive exclusion of N8 by 905 changed with the experimental temperature levels. R. raciborskii N8 showed a slight growth only at the beginning of 4 days at 16 °C, but a longer growth phase and higher biovolume were observed at 24 °C and 32 °C (Fig. 1). Although N8 biovolumes markedly increased under high temperature, they dropped after reaching maximum value on the 14th day and the strain 905 completely dominated at the end of the experiments (Fig. 1).

In the competition experiments between 915 and N8 under three temperature levels, the competitive outcomes between two species were variable. 915 and N8 were able to coexist at 16 °C and 32 °C, but 915 competitively excluded N8 at 24 °C (Fig. 2). M. aeruginosa FACHB915 showed a strong competitive ability at 24 °C and displaced R. raciborskii N8 from day 14. At 16 °C and 32 °C, the biovolumes of both species increased, but M. aeruginosa FACHB915 increased with a higher growth rate in the mixed population (Fig. 2). Hence, we observed a shift of 1:30 initial ratio towards ratio 1:8.8 (16 °C) and 1:1.6 (32 °C) at the end of the experiments.

In the competition experiments between 469 and N8 under three temperature levels, two species coexisted, but their relative dominance was significantly affected by temperature (Fig. 3). At 16 °C, both species increased with a similar growth rate and the biovolume ratio between 469 and N8 was still kept around 1:30 at the end of the experiment (Fig. 3). At 24 °C, M. aeruginosa FACHB469 increased with a higher growth rate in the mixed population and its relative contribution in total biovolume showed a significant increase from 3.3% of day 1 to 47.6% of day 31 (Fig. 3). At 32 °C, both species increased with a similar growth rate until the twenty-second day and then M. aeruginosa FACHB469 slightly increased its growth rate. Therefore, with an initial advantage, R. raciborskii N8 showed a slight decrease (from 96.7% to 91.7%) in its relative proportion and was still able to maintain its dominance at 32 °C (Fig. 3).

For each species pair, we calculated rates of competitive exclusion (RCE) according to Grover (1991), as the slope of the linear regression of ln (Microcystis biovolume/Raphidiopsis biovolume) with time. One-way ANOVA test showed the RCD values of the same species pair were significantly different at three temperature levels (P < 0.05). The RCD values confirmed that M. aeruginosa gained the advantage under most of experimental conditions and all three strains excluded R. raciborskii N8 at a much faster rate at 24 °C (Tab. 1). Under the same temperature, the RCD was always highest for Microcystis FACHB905 and lowest for Microcystis FACHB469.

thumbnail Fig. 1

Time course of the biovolumes of M. aeruginosa FACHB905 and R. raciborskii N8 in the competition experiments at 16 °C, 24 °C and 32 °C.
thumbnail Fig. 2

Time course of the biovolumes of M. aeruginosa FACHB915 and R. raciborskii N8 in the competition experiments at 16 °C, 24 °C and 32 °C.
thumbnail Fig. 3

Time course of the biovolumes of M. aeruginosa FACHB469 and R. raciborskii N8 in the competition experiments at 16 °C, 24 °C and 32 °C.
Table 1

Rates of competition exclusion (RCE) for each species pair under three temperature levels.

3.2 R. raciborskii N8 growth changing with MC-LR concentrations

Compared to the control (0 µg L−1 MC-LR), R. raciborskii N8 incubated with different MC-LR concentrations increased rapidly and grew well during the whole experimental periods (Fig. 4). Although chla concentrations of R. raciborskii at stationary phase slightly changed, the difference between the control and treatments was not significant (P > 0.05).

thumbnail Fig. 4

Growth curves of R. raciborskii N8 incubated with MC-LR.

3.3 R. raciborskii N8 growth in spent medium of M. aeruginosa FACHB905

Spent medium of M.aeruginosa FACHB905 had a concentration-related effect on the growth of R. raciborskii N8 (Fig. 5). Compared to the control (0% spent medium), 5 ∼ 50% spent medium resulted in a rapid decrease in both the chla concentrations (P < 0.05) and growth phase of R. raciborskii N8. Excellent growth was observed in both the control and 2.5% spent medium and there was no significant difference between them (P > 0.05; Fig. 5). In 5% spent medium, the biomass of R. raciborskii N8 increased and reached maximal concentrations of 73.4 µg L−1 at 11th day, and a 35% inhibition of R. raciborskii growth was observed at the end of experiment. The strongest inhibition (up to 96%) on growth of R. raciborskii N8 was observed in the treatments with 40% and 50% spent medium.

thumbnail Fig. 5

Growth curves of R. raciborskii N8 in BG11 with 0–50% spent medium of M. aeruginosa FACHB905.

3.4 R. raciborskii N8 growth in crude extract of M. aeruginosa FACHB905

All R. raciborskii groups incubated with six ratios of M. aeruginosa FACHB905 crude extract grew well during the whole experimental periods (Fig. 6). Although the chla concentrations of R. raciborskii at stationary phase slightly changed, the difference between the control and treatments was not significant (P > 0.05).

thumbnail Fig. 6

Growth curves of R. raciborskii N8 of in BG11 with 0–6.67% crude extract of M. aeruginosa FACHB905.

4 Discussion

Our findings highlight the strong variation in the competitiveness of three M. aeruginosa strains. M. aeruginosa FACHB905 was the most competitive, and can completely exclude R. raciborskii N8 in the competition experiments. The other two strains of M. aeruginosa can coexist with R. raciborskii, but the strain FACHB915 is more competitive than FACHB469. Our study confirms the previous findings that Microcystis isolated from the same or different water bodies are strain-specific and diverse in phenotypes, genotypes and chemotypes (Welker et al., 2004; Haande et al., 2007; Alexova et al., 2011; Yang et al., 2015; Xiao et al., 2017a). The high plasticity of Microcystis strains led to considerable variation in their responses to environmental conditions. Therefore, the competition outcomes between M. aeruginosa and R. raciborskii were highly uncertain (Marinho et al., 2013; Xiao et al., 2017b; da Silva Brito et al., 2018).

Some studies demonstrated that it was unlikely to generalize the environmental conditions in which one species/strain may dominate because biological differences between cyanobacterial strains significantly affected growth responses to environmental conditions. When exposed to different light or phosphate limitation, R. raciborskii can either dominate or be displaced by M. aeruginosa (Marinho et al., 2013). da Silva Brito et al. (2018) found that M. aeruginosa dominated under conditions of high alkalinity and high pH but was overcome by R. raciborskii under conditions of low alkalinity and lower pH. When exposed to compounds produced by R. raciborskii, all M. aeruginosa strains but LEA-04 formed colony, indicating that specificity played a role in the interaction between two species (Mello et al., 2012) These results supported the argument that cyanobacterial competition was highly variable, depending on strains and environmental conditions (Marinho et al., 2013; Xiao et al., 2017b).

Competition between phytoplankton species can include an active process defined as allelopathy (Rice, 1984; Leão et al., 2009). Several previous studies showed that toxic M. aeruginosa FACHB905 had a strong inhibitory effects on growth of other phytoplankton species such as non-toxic M. aeruginosa FACHB469, M. wesenbergii, Aphanizomenon flos-aquae, Chlorella vulgaris, Chlorella pyrenoidosa, Scenedesmus quadricauda, and Cyclotella meneghiniana (Yang et al., 2014; Lei et al., 2015; Ma et al., 2015a; Ma et al., 2015b; Wang et al., 2017). In this study, we observed a complete exclusion of M. aeruginosa FACHB905 against R. raciborskii N8 in the competition experiments, even if the initial ratio of their biovolumes was as high as 1:1800. The extreme competitive ability of FACHB905 may significantly attribute to its allelopathic effects on other phytoplankton species (Yang et al., 2014; Lei et al., 2015; Ma et al., 2015a; Ma et al., 2015b; Wang et al., 2017). MCs was considered as allelopathic compounds that allow toxic Microcystis strains to inhibit the growth of their competitors in phytoplankton communities (Sedmak and Elersek, 2005; Leão et al., 2009). Yang et al. (2014) put forward that both MC and other allelopathic compounds in M. aeruginosa FACHB905 had synergistic effects on inhibition of M. wesenbergii. However, a bioassay with pure MC-LR with concentrations of 250 µg L−1 and 500 µg L−1 did not inhibit the growth of A. flos-aquae (Ma et al., 2015a), and our results were consistent with the above investigation that no significant difference of R. raciborskii growth was observed between the control and treatment with 0.1–1000 µg L−1 MC-LR. Thus MC-LR was excluded as a candidate allelopathic compound and there existed other unknown secondary metabolites responsible for the allelopathic effects of M. aeruginosa FACHB905 (Yang et al., 2014; Ma et al., 2015a).

Allelopathy has been suggested to be an important explanation for mediating the seasonal dynamics of different cyanobacterial species (Figueredo et al., 2007). Cyanobacteria are known to produce a variety of secondary metabolites with potent biological activities, some of which have been released into the surrounding medium as allelopathic compounds aiding in interspecific competition (Leão et al., 2009, 2010). Cylindrospermosin and an unknown bioactive compound secreted by R. raciborskii can inhibit the growth of M. aeruginosa, and thus contribute to the stable dominance of R. raciborskii (Figueredo et al., 2007; Mello et al., 2012; Rzymski et al., 2014). Conversely, our results showed that the growth of R. raciborskii N8 was significantly inhibited by M. aeruginosa FACHB905, indicating that the chemically mediated process between R. raciborskii and M. aeruginosa was mutual and interactive. The findings that the growth inhibition was induced by spent medium of M. aeruginosa FACHB905 but not by its crude extracts demonstrated that allelopathic compounds were extracellularly released. Several studies have also confirmed that allelopathic effects of M. aeruginosa FACHB905 on other phytoplankton species were from its filtrates or exudates (Yang et al., 2014; Ma et al., 2015a; Wang et al., 2017). Yang et al. (2014) tried to characterize allelopathic compounds from this strain with GC-MS and an unknown compound of molecular weight 678.4 was found. However, the exact chemical structure of the compound remains unclear.

Changes in environmental factors can also affect the competition outcomes between M. aeruginosa and R. raciborskii. Temperature is one of crucial environmental factors regulating bloom development and phytoplankton succession. Many studies have demonstrated that rising temperature can promote the growth and spread of invasive species of R. raciborskii, and thus likely favor these cyanobacteria over the native species M. aeruginosa (O'Neil et al., 2012; Thomas and Litchman, 2016). In the present study, we found that temperature has a large impact on the competition between three M. aeruginosa strains and R. raciborskii N8. In 905 & N8 co-cultures, although M. aeruginosa was absolutely a winner at the end of the experiment, the growth of R. raciborskii obviously increased with elevated temperatures. In the competition experiments for 915 and N8, M. aeruginosa almost excluded R. raciborskii at 24 °C but coexisted until the end of the experiment at 16 °C and 32 °C. M. aeruginosa FACHB469 also showed a strong competitiveness at 24 °C and increased its percentage from 3.3% to 47.6%. Therefore, M. aeruginosa species can dominate over or outcompete R. raciborskii at 24 °C, while R. raciborskii maintained its initial advantage at 16 °C and 32 °C, indicating that rising temperatures can better promote the growth of R. raciborskii. Our result was similar to previous study that the dominant strain in cyanobacterial competition always was the species M. aeruginosa at 20 °C and R. raciborskii at 28 °C (Xiao et al., 2017b).

5 Conclusion

In conclusion, our experiments showed that there existed physiological variation between M. aeruginosa strains, and thus the competition outcome between M. aeruginosa and R. raciborskii were highly variable. M. aeruginosa FACHB905 was the strongest competitor and almost excluded R. raciborskii, while M. aeruginosa FACHB469 was the weakest one and always coexisted with R. raciborskii. Temperature has a significant influence on the competition between the two species. M. aeruginosa outcompeted R. raciborskii at 24 °C, while R. raciborskii maintained its initial advantage at 16 °C and 32 °C. In order to predict the development of cyanobacteria bloom, physiological difference between strains should be considered as well as environmental conditions.

Acknowledgements

This work was funded by a National Natural Science Foundation of China (NSFC) grant (No. 31770507) and the Water Resource Science and Technology Innovation Program of Guangdong Province (Grant No. 2016-29).

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Cite this article as: Lei L, Dai J, Lin Q, Peng L. 2020. Competitive dominance of Microcystis aeruginosa against Raphidiopsis raciborskii is strain- and temperature-dependent. Knowl. Manag. Aquat. Ecosyst., 421, 36.

Supplementary Material

Supplementary Figure S1. (Access here)

All Tables

Table 1

Rates of competition exclusion (RCE) for each species pair under three temperature levels.

In the text

All Figures

thumbnail Fig. 1

Time course of the biovolumes of M. aeruginosa FACHB905 and R. raciborskii N8 in the competition experiments at 16 °C, 24 °C and 32 °C.
In the text
thumbnail Fig. 2

Time course of the biovolumes of M. aeruginosa FACHB915 and R. raciborskii N8 in the competition experiments at 16 °C, 24 °C and 32 °C.
In the text
thumbnail Fig. 3

Time course of the biovolumes of M. aeruginosa FACHB469 and R. raciborskii N8 in the competition experiments at 16 °C, 24 °C and 32 °C.
In the text
thumbnail Fig. 4

Growth curves of R. raciborskii N8 incubated with MC-LR.
In the text
thumbnail Fig. 5

Growth curves of R. raciborskii N8 in BG11 with 0–50% spent medium of M. aeruginosa FACHB905.
In the text
thumbnail Fig. 6

Growth curves of R. raciborskii N8 of in BG11 with 0–6.67% crude extract of M. aeruginosa FACHB905.
In the text

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