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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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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) 24:46664675
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. ...
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