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Allelopathic effect boosts Chrysosporum ovalisporum dominance in summer at the expense of Microcystis panniformis in a shallow coastal water body

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Wei Zhang at Shanghai Ocean University
Wei Zhang
Erik Jeppesen at Aarhus University
Erik Jeppesen
Mengmeng Wang
Mengmeng Wang
Mengmeng Wang
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Xiaoying Xu
Xiaoying Xu
Xiaoying Xu
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Abstract and Figures

The increased occurrence of harmful cyanobacterial species and, with this, higher frequency of cyanobacteria blooms, closely associated with eutrophication and climate change, have attracted increasing attention worldwide. However, competition mechanisms between the different bloom-forming cyanobacteria species remain to be elucidated. In this paper, for the first time, the allelopathic effect of the cyanobacterium Chrysosporum ovalisporum on the cyanobacterium Microcystis panniformis is reported. The results of our study conducted in a Chinese shallow coastal water body demonstrated that the biomass of M. panniformis was relatively low during the C. ovalisporum blooming period. Co-cultivation of a C. ovalisporum strain with a M. panniformis strain showed strong inhibition of the growth of M. panniformis but stimulation of C. ovalisporum. Thus, filtrate of C. ovalisporum culture had a strong inhibitory effect on the performance of M. panniformis by decreasing the maximum optical quantum yield (Fv/Fm), the electron transport rate (ETR) of PS II and the onset of light saturation (Ik) and by increasing the alkaline phosphatase (ALP) activity and superoxide dismutase (SOD) activity of M. panniformis. Our results suggest that the interspecific allelopathic effect plays an important role in the competition between different cyanobacteria species. We foresee the importance of C. ovalisporum to intensify in a future warmer world, not least in small- to medium-sized, warm and high conductivity coastal water bodies.
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RESEARCH ARTICLE
Allelopathic effect boosts Chrysosporum ovalisporum dominance
in summer at the expense of Microcystis panniformis in a shallow
coastal water body
Wei Zhang
1
&Erik Jeppesen
2,3
&Mengmeng Wang
1
&Xiaoying Xu
1
&Liqing Wang
1
Received: 24 August 2016 /Accepted: 23 November 2016 /Published online: 14 December 2016
#Springer-Verlag Berlin Heidelberg 2016
Abstract The increased occurrence of harmful cyanobacterial
species and, with this, higher frequency of cyanobacteria
blooms, closely associated with eutrophication and climate
change, have attracted increasing attention worldwide.
However, competition mechanisms between the different
bloom-forming cyanobacteria species remain to be elucidated.
In this paper, for the first time, the allelopathic effect of the
cyanobacterium Chrysosporum ovalisporum on the cyanobac-
terium Microcystis panniformis is reported. The results of our
study conducted in a Chinese shallow coastal water body dem-
onstrated that the biomass of M. panniformis was relatively low
during the C. ovalisporum blooming period. Co-cultivation of a
C. ovalisporum strain with a M. panniformis strain showed
strong inhibition of the growth of M. panniformis but stimula-
tion of C. ovalisporum. Thus, filtrate of C. ovalisporum culture
had a strong inhibitory effect on the performance of
M. panniformis by decreasing the maximum optical quantum
yield (F
v
/F
m
), the electron transport rate (ETR) of PS II and the
onset of light saturation (I
k
) and by increasing the alkaline
phosphatase (ALP) activity and superoxide dismutase (SOD)
activity of M. panniformis. Our results suggest that the inter-
specific allelopathic effect plays an important role in the com-
petition between different cyanobacteria species. We foresee
the importance of C. ovalisporum to intensify in a future warm-
er world, not least in small- to medium-sized, warm and high
conductivity coastal water bodies.
Keywords Allelopathy .Chrysosporum ovalisporum .
Microcystis panniformis .Competition .
Cylindrospermopsin .Bloom
Introduction
For multiple decades, competition between phytoplankton
species has been an important topic within aquatic ecology
(Sommer 1989; Wacker et al. 2015). Phytoplankton species
compete for resources through different physiological adapta-
tions (e.g. photosynthetic capacity, nutrient requirement, lux-
ury uptake, mixotrophy and degree of vertical migration)
(Huisman et al. 2004; Legrand et al. 2003;Torresetal.
2015). Also, allelopathy, i.e. the beneficial or harmful effects
of one plant on another plant, is known to be an important
ecological adaptation mechanism employed by phytoplankton
(Legrand et al. 2003). Via secondary metabolites, some phy-
toplanktonspecies may compete successfully with their oppo-
nents (Leflaive and Ten-Hage 2007; Sukenik et al. 2002), and
allelopathy is, therefore, considered an important factor in the
species succession and formation of algal blooms (Bar-Yosef
et al. 2010;Princeetal.2008).
Although allelopathy is acknowledged for its importance,
specific knowledge about its effects remains limited. Several
studies have revealed that secondary metabolites may inhibit
photosynthesis and enzyme activity and produce oxidative
stress (Leflaive and Ten-Hage 2007;Princeetal.2008;
Sukenik et al. 2002). However, a growing number of studies
Responsible editor: Vitor Manuel Oliveira Vasconcelos
Electronic supplementary material The online version of this article
(doi:10.1007/s11356-016-8149-0) contains supplementary material,
which is available to authorized users.
*Liqing Wang
lqwang@shou.edu.cn
1
College of Fisheries and Life Science, Shanghai Ocean University,
Shanghai, China
2
Department of Bioscience, Aarhus University, Silkeborg, Denmark
3
Sino-Danish Centre for Education and Research (SDC),
Beijing, China
Environ Sci Pollut Res (2017) 24:4666–4675
DOI 10.1007/s11356-016-8149-0
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Non-diazotrophic blooms were much smaller in magnitude (by a factor >10) and were rarely concurrent with the C. ovalisporum bloom. Zhang et al. (2017) observed similar trends in Lake Dishui, China. C. ovalisporum formed high biomass blooms during warmer temperatures, followed by smaller magnitude blooms of Microcystis panniformis. ...
... C. ovalisporum formed high biomass blooms during warmer temperatures, followed by smaller magnitude blooms of Microcystis panniformis. The results of a series of competition experiments also suggested that C. ovalisporum inhibited Microcystis growth through an allelopathic effect (Shao et al., 2013;Zhang et al., 2017). Similar allelopathic interactions at Mannus Lake may explain community succession patterns and the much lower biomass of the non-diazotrophic blooms, however further research is required on allelopathic interactions between cyanobacteria (Zhang et al., 2017). ...
... The results of a series of competition experiments also suggested that C. ovalisporum inhibited Microcystis growth through an allelopathic effect (Shao et al., 2013;Zhang et al., 2017). Similar allelopathic interactions at Mannus Lake may explain community succession patterns and the much lower biomass of the non-diazotrophic blooms, however further research is required on allelopathic interactions between cyanobacteria (Zhang et al., 2017). Another likely explanation is that bloom events at Mannus Lake are driven by different environmental conditions. ...
Severe cyanobacterial blooms in an Australian lake; causes and factors controlling succession patterns
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Cyanobacterial blooms have major impacts on the ecological integrity and anthropogenic value of freshwater systems. Chrysosporum ovalisporum, a potentially toxic cyanobacteria has been rare in Australian waters until recently when is has bloomed in a number of lake and river systems. The aim of this study was to determine drivers of its growth and growing dominance. We performed regular monitoring of Mannus Lake, a small freshwater reservoir in South-Eastern Australia that has recently undergone extremely dense bloom events. Blooms of the diazotrophic Chrysosporum ovalisporum occurred in both summers of the 19 month study during periods of persistent thermal stratification. Following the C. ovalisporum blooms, non-diazotrophic taxa (Microcystis aeruginosa and Woronichinia sp.) dominated the phytoplankton community under less stratified conditions. Thermal stratification and nitrogen availability appeared to be the primary drivers of changes in cyanobacterial community structure. We propose that the observed transition from C. ovalisporum to M. aeruginosa and/or Woronichinia sp. may be a result of nitrogen limitation in early summer, which combined with persistent thermal stratification led to an ecological advantage for the nitrogen-fixing C. ovalisporum. Mixing events caused the senescence of the C. ovalisporum bloom, likely supplementing the nutrient budget of the lake with atmospherically derived N and alleviating N limitation to non-diazotrophic taxa. Non-diazotrophic cyanobacterial growth then increased, albeit at much lower biovolumes compared to the initial bloom. Overall, the results demonstrate the role of thermal stratification and nutrient cycling in structuring the cyanobacterial community and provide insights into the environmental factors driving the proliferation of the relatively new, potentially toxic cyanobacterium C. ovalisporum in Australian waters.
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... In recent years, other cyanobacteria with a strong dispersal ability and invasive potential have been observed to develop blooms, e.g. in Chinese rivers, lakes, and reservoirs (Jiang et al., 2014;Lei et al., 2014). Among these, CYN-producing Cylindrospermopsis and Chrysosporium have attracted special attention (Fadel et al., 2014;Burford et al., 2016;Zhang et al., 2017) as they have shown strong competitiveness and may replace Microcystis under certain conditions (Lei et al., 2014;Zhang et al., 2017), in part as result of CYN production . Several studies have focused on the impact of CYN on various aquatic organisms. ...
... In recent years, other cyanobacteria with a strong dispersal ability and invasive potential have been observed to develop blooms, e.g. in Chinese rivers, lakes, and reservoirs (Jiang et al., 2014;Lei et al., 2014). Among these, CYN-producing Cylindrospermopsis and Chrysosporium have attracted special attention (Fadel et al., 2014;Burford et al., 2016;Zhang et al., 2017) as they have shown strong competitiveness and may replace Microcystis under certain conditions (Lei et al., 2014;Zhang et al., 2017), in part as result of CYN production . Several studies have focused on the impact of CYN on various aquatic organisms. ...
The effect of cylindrospermopsin on the bacterioplankton community: a microcosm experiment on water from Dishui Lake, Shanghai, China
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Eutrophication and climate warming have intensifi ed the global expansion of invasive cyanobacteria such as Cylindrospermopsis spp. and Chrysosporum spp. Cylindrospermopsin (CYN) produced by species of the latter two genera may harm phytoplankton, zooplankton, and fi shes. However, eff ects of CYN on the bacterioplankton community have not been studied. Based on high-throughput sequencing, we explored the eff ect of CYN on the structure and function of the bacterioplankton community by adding pure CYN to in-situ water collected from a brackish coastal shallow lake: Dishui Lake, China. We found that most bacterioplankton taxa had a certain tolerance potential to CYN, but that high concentrations of CYN (40 μg/L) caused a signifi cant decrease in microbial abundance and functional groups. Of the dominant phyla, Actinobacteria had the strongest tolerance to CYN. Network analysis indicated that CYN caused shifts in the community structure of the bacterioplankton, reducing community stability and structural complexity. High CYN concentrations also reduced the correlation between the diff erent bacterioplankton groups, and the abundances of some bacterial taxa associated with the denitrifi cation function and the process of carbon transfer in the microbial food web were inhibited. Our study provides new insight into the response of the bacterioplankton communities to harmful algal toxins produced by cyanobacteria.
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... The culture duration was nine days, and each sample was counted six times to derive an average value. The specific growth rate (μ) was determined by cell densities according to the following equation [25]: where X 1 is the algal cell density at the initial incubation time point (T 1 ) and X 2 is the cell density at the end time point (T 2 ). ...
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... For the sampling and determination of experimental samples, 1 mL of the shaken algal solution to be measured was filtered through a 0.22-μm sterile filter tip into a 1.5-mL injection bottle, and stored in a refrigerator at − 20 °C, protected from light, to determine the concentration of ENR by using a high-performance liquid chromatograph (HPLC, Agilent 1100, USA) (Roháček and Barták 1999;Zhang et al. 2017). ...
Linking the removal of enrofloxacin to the extracellular polymers of microalgae in water bodies: A case study focusing on the shifts in microbial communities
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Microalgae can promote antibiotic removal, which has attracted growing attention. However, its synergistic removal performance with bacteria in antibiotic pollutants is still poorly understood. In this study, firstly, we selected two green algae (Dictyosphaerium sp. and Chlorella sp.) and exposed them to Enrofloxacin (ENR) to observe their extracellular polysaccharides (EPS) concentration dynamic and the removal of antibiotics. Secondly, EPS was extracted and added to in situ lake water (no algae) to investigate its combined effect with bacteria. The results indicate that both Dictyosphaerium sp. and Chlorella sp. exhibited high tolerance to ENR stress. When the biomass of microalgae was low, ENR could significantly stimulate algae to produce EPS. The removal rates of Dictyosphaerium sp. and Chlorella sp. were 15.8% and 10.5%, respectively. The addition of EPS can both alter the microbial community structure in the lake water and promote the removal of ENR. The LEfSe analysis showed that there were significant differences in the microbial marker taxa, which promoted the increase of special functional bacteria for decomposing ENR, between the EPS-added group and the control group. The EPS of Dictyosphaerium sp. increased the abundance of Moraxellaceae and Spirosomaceae, while the EPS of Chlorella sp. increased the abundance of Sphingomonadaceae and Microbacteriaceae. Under the synergistic effect, Chlorella sp. achieved a maximum removal rate of 24.2%, while Dictyosphaerium sp. achieved a maximum removal rate of 28.9%. Our study provides new insights into the removal performance and mechanism of antibiotics by freshwater microalgae in water bodies and contribute to the development of more effective water treatment strategies.
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... It was supplemented by Rise in his book Allelopathy in 1974 [9] and in the reprint of Allelopathy in 1984 [10]. Allelopathy refers to the interactions between plants [11,12], plants and microorganisms [13,14], and microorganisms and microorganisms [15,16]. The modes of action include promotion and inhibition [17,18]. ...
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... 34.9. C. ovalisporum has also been reported from a wide range of salinities from Spain 1756 (Quesada et al., 2006), Shanghai 178-5905 (Zhang et al., 2017), and Turkey 900-1056 (Akcaalan et al., 2014). In Southeastern Australia blooms of C. ovalisporum were reported from slightly brackish artificial lakes with conductivity ranging between 1650 and 3550 , and in a stratified artificial lake, conductivity ranged between 344 and 2290 in different strata (Everson et al., 2009). ...
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Continuous-release beads of natural allelochemicals for the long-term control of cyanobacterial growth: Preparation, release dynamics and inhibitory effects
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Interspecific competition in phytoplankton drives the availability of essential mineral and biochemical nutrients
Article
  • Sep 2015
The underlying mechanisms and consequences of competition and diversity are central themes in ecology. A higher diversity of primary producers often results in higher resource use efficiency in aquatic and terrestrial ecosystems. This may result in more food for consumers on one hand, while, on the other hand, it can also result in a decreased food quality for consumers; higher biomass combined with the same availability of the limiting compound directly reduces the dietary proportion of the limiting compound. Here we tested whether and how interspecific competition in phytoplankton communities leads to changes in resource use efficiency and cellular concentrations of nutrients and fatty acids. The measured particulate carbon : phosphorus ratios (C:P) and fatty acid concentrations in the communities were compared to the theoretically expected ratios and concentrations of measurements on simultaneously running monocultures. With interspecific competition, phytoplankton communities had higher concentrations of the monounsaturated fatty acid oleic acid and also much higher concentrations of the ecologically and physiologically relevant long-chain polyunsaturated fatty acid eicosapentaenoic acid than expected concentrations based on monocultures. Such higher availability of essential fatty acids may contribute to the positive relationship between phytoplankton diversity and zooplankton growth, and may compensate limitations by mineral nutrients in higher trophic levels.
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Allelopathic effect between Microcystis aeruginosa and three filamentous cyanobacteria
Article
  • Jan 2006
Allelopathy, the release of extracellular compounds that have an effect on the growth of other microorganisms, may be one factor contributing to formation and/or maintenance of cyanobacterial blooms. In this paper, the allelopathic effect between single-cell Microcystis aeruginosct and three filamentous cyanobacteria助hanizomerznn flos-uquae, Anabaena flos-aqtuae, Phormidium mucicolu was investigated. The experiment was conducted to find out the allelopathic effects of cell-free filtrate on the growth of different target organisms; 1.the cell-free filtrate of M.uPruginnsa on Aphunizomenorz flos-aquue, Arzubaerz.a fins-aquae and P. mucicola;2. the cell-free filtrate of Aphurztzomenon flos-uquae, Arzabuena flos-aquae and P. mucicola on M. aeruginosu. The results demonstrated that M.ueruginosu could accelerate the growth of Aphanizontenorz flo.s-rzquae and Anahrzerza flos-uquae, and slightly inhibited P. ntucicola. On the other hand, the growth of M, deruginostx was slightly suppressed by Aphurzizumenorz fins-aquue and.4rzabaena flo.s-aquae, but heavily inhibited by P. mucicolu. The inhibition by P. ntucicolu was enhanced with thf; increase of concentration of cell-free filtrate. Furthermore, the allelopathic effect between single-cell M. uerugino.su and three filamentons cyanobacteria.9phurzizurrzertnn flos-uquoe, Atwbaena floc-aquue, P. mucicolu was not influenced by the change of the concentration of inorganic nutrients in cell-free filtrates. It suggests that the inter-speties competition existed in cyanobacteria. The present study is implicated in illustrating dynamics of the cyanobacserial bloom.
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Nutrient status and nutrient competition of phytoplankton in a shallow, hypertrophic lake
Article
  • Nov 1989
The nutritional status of phytoplankton in a shallow, hypertrophic lake was analyzed by stoichiometry of seston and by enrichment bioassays during a 6‐month period. Both methods suggested moderate and temporally interrupted nutrient limitation of reproductive rates. Nitrogen was the most frequently limiting nutrient, phosphorus was next, and silicate limitation of three diatom species occurred only once. The nutritional status of the most abundant individual species could be described by the Monod equation. The nutritional status of the entire phytoplankton assemblage could be described by a modified version of the Droop equation. In accordance with competition theory, phytoplankton species were arrayed along resource ratio gradients. These results are consistent with ecophysiological models derived from culture experiments.
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