Grazing of the copepod Cyclops vicinus on toxic Microcystis aeruginosa: potential for controlling cyanobacterial blooms and transfer of toxins

Abstract Grazing of zooplankton on phytoplankton may contribute to a reduction of harmful cyanobacteria in eutrophic waters. However, the feeding capacity and interaction between zooplankton and toxic cyanobacteria vary among grazer species. In this study, laboratory feeding experiments were designed to measure the grazing rate of the copepod Cyclops vicinus on Microcystis aeruginosa and the potential microcystin (MC) accumulation in the grazer. Copepods were fed a mixed diet of the edible green alga Ankistrodesmus falcatus and toxic M. aeruginosa for 10 days. The results showed that C. vicinus efficiently ingested toxic Microcystis cells with high grazing rates, varying during the feeding period (68.9–606.3 Microcystis cells animal-1 d-1) along with Microcystis cell density. Microcystis cells exhibited a remarkable induction in MC production under grazing conditions with concentrations 1.67–12.5 times higher than those in control cultures. Furthermore, C. vicinus was found to accumulate MCs in its body with concentrations increasing during the experiment (0.05–3.21 μg MC animal-1). Further in situ studies are needed to investigate the ability of Cyclops and other copepods to assimilate and detoxify MCs at environmentally relevant concentrations before deciding on the biocontrol of Microcystis blooms by copepods.

Download Full-text

Physiological and Metabolic Responses of Marine Mussels Exposed to Toxic Cyanobacteria Microcystis aeruginosa and Chrysosporum ovalisporum

Toxins ◽

10.3390/toxins12030196 ◽

2020 ◽

Vol 12 (3) ◽

pp. 196 ◽

Cited By ~ 1

Author(s):

Flavio Oliveira ◽

Leticia Diez-Quijada ◽

Maria V. Turkina ◽

João Morais ◽

Aldo Barreiro Felpeto ◽

...

Keyword(s):

Microcystis Aeruginosa ◽

Dry Weight ◽

Cyanobacterial Blooms ◽

Control Group ◽

Freshwater Bivalve ◽

Marine Mussel ◽

Toxic Cyanobacteria ◽

Parachlorella Kessleri ◽

Marine Mussels ◽

Exposure Experiment

Toxic cyanobacterial blooms are a major contaminant in inland aquatic ecosystems. Furthermore, toxic blooms are carried downstream by rivers and waterways to estuarine and coastal ecosystems. Concerning marine and estuarine animal species, very little is known about how these species are affected by the exposure to freshwater cyanobacteria and cyanotoxins. So far, most of the knowledge has been gathered from freshwater bivalve molluscs. This work aimed to infer the sensitivity of the marine mussel Mytilus galloprovincialis to single as well as mixed toxic cyanobacterial cultures and the underlying molecular responses mediated by toxic cyanobacteria. For this purpose, a mussel exposure experiment was outlined with two toxic cyanobacteria species, Microcystis aeruginosa and Chrysosporum ovalisporum at 1 × 105 cells/mL, resembling a natural cyanobacteria bloom. The estimated amount of toxins produced by M. aeruginosa and C. ovalisporum were respectively 0.023 pg/cell of microcystin-LR (MC-LR) and 7.854 pg/cell of cylindrospermopsin (CYN). After 15 days of exposure to single and mixed cyanobacteria, a depuration phase followed, during which mussels were fed only non-toxic microalga Parachlorella kessleri. The results showed that the marine mussel is able to filter toxic cyanobacteria at a rate equal or higher than the non-toxic microalga P. kessleri. Filtration rates observed after 15 days of feeding toxic microalgae were 1773.04 mL/ind.h (for M. aeruginosa), 2151.83 mL/ind.h (for C. ovalisporum), 1673.29 mL/ind.h (for the mixture of the 2 cyanobacteria) and 2539.25 mL/ind.h (for the non-toxic P. kessleri). Filtering toxic microalgae in combination resulted in the accumulation of 14.17 ng/g dw MC-LR and 92.08 ng/g dw CYN. Other physiological and biochemical endpoints (dry weight, byssus production, total protein and glycogen) measured in this work did not change significantly in the groups exposed to toxic cyanobacteria with regard to control group, suggesting that mussels were not affected with the toxic microalgae. Nevertheless, proteomics revealed changes in metabolism of mussels related to diet, specially evident in those fed on combined cyanobacteria. Changes in metabolic pathways related with protein folding and stabilization, cytoskeleton structure, and gene transcription/translation were observed after exposure and feeding toxic cyanobacteria. These changes occur in vital metabolic processes and may contribute to protect mussels from toxic effects of the toxins MC-LR and CYN.

Download Full-text

Occurrence of potentially toxic cyanobacteria Microcystis aeruginosa in aquatic ecosystems of central Kerala (south India)

Annales de Limnologie - International Journal of Limnology ◽

10.1051/limn/2020015 ◽

2020 ◽

Vol 56 ◽

pp. 18

Author(s):

Renju Mohan ◽

Twinkle Sathish ◽

Kunnatholickal Balakrishnan Padmakumar

Keyword(s):

Microcystis Aeruginosa ◽

Aquatic Ecosystems ◽

South India ◽

Early Summer ◽

Cyanobacterial Blooms ◽

Fish Mortality ◽

Freshwater Ponds ◽

Toxic Cyanobacteria ◽

Toxicological Studies ◽

Major Factors

Microcystis aeruginosa is a potentially toxic bloom-forming freshwater cyanobacterium, usually found in eutrophic water bodies worldwide. The present study reports the occurrence of Microcystis aeruginosa and its bloom in freshwater ponds along central Kerala (south India). Monitoring of cyanobacterial blooms was conducted from May 2019 to February 2020 along the aquatic ecosystems of central Kerala and the M. aeruginosa blooms were recorded from two freshwater ponds of Kochi. Massive blooms of M. aeruginosa was observed during the period prior to summer monsoon (May) with an abundance of 1.17 × 106 cells L‑1 (Station 1) and during early summer (February) latter being more thick scum (2 × 108 cells L‑1) with high chlorophyll a. Dense aggregates of M. aeruginosa scums were more prevalent during the periods characterised by higher Surface Water Temperature (SWT). The nutrient characteristic pattern of the study area showed the abundance of M. aeruginosa correlated very well with higher dissolved nitrate (96.7 μmol L‑1) and phosphate (19.88 μmol L‑1) concentrations. Thus in the stable freshwater ponds with higher SWT and nutrients were the major factors influencing the growth and abundance of the cyanobacteria M. aeruginosa. Toxicological studies conducted revealed that the Microcystis bloom was hepatotoxic, inflicting fish mortality.

Download Full-text

Allelopathic effects of the aquatic macrophyte Ceratophyllum demersum L. on phytoplankton species: contrasting effects between cyanobacteria and chlorophytes

Acta Limnologica Brasiliensia ◽

10.1590/s2179-975x1419 ◽

2019 ◽

Vol 31 ◽

Cited By ~ 6

Author(s):

Cihelio Alves Amorim ◽

Rafael Henrique de Moura-Falcão ◽

Celina Rebeca Valença ◽

Vitor Ricardo de Souza ◽

Ariadne do Nascimento Moura

Keyword(s):

Microcystis Aeruginosa ◽

Growth Rates ◽

Culture Medium ◽

Aquatic Macrophyte ◽

Cyanobacterial Blooms ◽

Ceratophyllum Demersum ◽

Phytoplankton Species ◽

Raphidocelis Subcapitata ◽

Ankistrodesmus Falcatus ◽

Allelopathic Effects

Abstract Aim To assess the allelopathic effects of the submerged macrophyte Ceratophyllum demersum on four strains of phytoplankton species: two cyanobacteria (Microcystis aeruginosa - microcystin producing and M. panniformis - non-microcystin producing), and two chlorophytes (Ankistrodesmus falcatus and Raphidocelis subcapitata). Methods A coexistence experiment between C. demersum and the four strains was carried out for six days, with eight treatments and three replicates. The strains were cultivated in ASM1 culture medium, under controlled laboratory conditions. Two treatments were assigned for each strain, one with 6 g.L-1 of the macrophyte, and the control without the plant. Biomasses and growth rates of the strains were evaluated every two days, which were compared through the T-test and two-way ANOVA, respectively. Results The results varied among the strains, with toxic M. aeruginosa being intensely inhibited by C. demersum, with a decrease of 99.5% in its biomass (p<0.001), while non-toxic M. panniformis was less affected by the allelochemicals, with a reduction of 86.2% (p<0.001). Ankistrodesmus falcatus delayed its growth when in coexistence with the macrophyte, decreasing its biomass in 50.4% (p<0.01), while R. subcapitata was not altered (p>0.05). In coexistence with C. demersum, M. aeruginosa exhibited the lowest growth rates (-0.65 d-1), followed by M. panniformis (-0.15 d-1), A. falcatus (0.19 d-1), and R. subcapitata (0.34 d-1), with significant differences between all strains (p<0.001). Microcystis aeruginosa presented higher inhibition rates than M. panniformis (p<0.001), as well as, A. falcatus was more inhibited than R. subcapitata (p<0.05). Conclusions The presence of microcystins could influence the allelopathic responses of C. demersum, that may release more allelochemicals in coexistence with toxic strains of M. aeruginosa. Accordingly, C. demersum can be used in biomanipulation strategies to control toxic and non-toxic cyanobacterial blooms, without damaging other phytoplankton species, like chlorophytes.

Download Full-text

Primary study on the feeding characteristics of a golden alga on Microcystis aeruginosa

Water Science & Technology ◽

10.2166/wst.2009.200 ◽

2009 ◽

Vol 59 (9) ◽

pp. 1727-1732

Author(s):

Xue Zhang ◽

Hong-Ying Hu ◽

Yu Hong

Keyword(s):

Microcystis Aeruginosa ◽

Growth Curve ◽

Algal Blooms ◽

Removal Rate ◽

Morphological Characters ◽

Primary Study ◽

Rdna Genes ◽

Feeding Experiments ◽

Toxic Cyanobacteria ◽

Short Time

A flagellate Jin821 which could feed on toxic cyanobacteria Microcystis aeruginosa was isolated, and it was identified as a species of golden alga according to its morphological characters and 18S rDNA genes. The results of feeding experiments showed that the golden alga Jin821 could make the high density (4.3 × 106 cells·mL−1) of M. aeruginosa clear in a short time (40 h), with a removal rate of 99.9%. And the microcystin (MC-LR) was also degraded effectively at the same time, with a removal rate of 82.7% of 114 μg/L in 40 h. The growth curve of Jin821 was in ‘S’ style, with four phases of lag, log, stationary and decline. When M. aeruginosa was cleaned out, Jin821 would decline in number and slowed down in movement. In summary, the golden alga Jin821 can be a potential biological way to control blue algal blooms in the future.

Download Full-text

Chemical Characterization of Microcystis aeruginosa for Feed and Energy Uses

Energies ◽

10.3390/en14113013 ◽

2021 ◽

Vol 14 (11) ◽

pp. 3013

Author(s):

Larissa Souza Passos ◽

Éryka Costa Almeida ◽

Claudio Martin Pereira de Pereira ◽

Alessandro Alberto Casazza ◽

Attilio Converti ◽

...

Keyword(s):

Microcystis Aeruginosa ◽

Animal Feed ◽

Renewable Energy Sources ◽

Chemical Characterization ◽

Cyanobacterial Blooms ◽

Energy Sources ◽

Carbohydrate Source ◽

Heating Value ◽

Adverse Health Effects ◽

Degradation Reactions

Cyanobacterial blooms and strains absorb carbon dioxide, drawing attention to its use as feed for animals and renewable energy sources. However, cyanobacteria can produce toxins and have a low heating value. Herein, we studied a cyanobacterial strain harvested during a bloom event and analyzed it to use as animal feed and a source of energy supply. The thermal properties and the contents of total nitrogen, protein, carbohydrate, fatty acids, lipid, and the presence of cyanotoxins were investigated in the Microcystis aeruginosa LTPNA 01 strain and in a bloom material. Microcystins (hepatotoxins) were not detected in this strain nor in the bloom material by liquid chromatography coupled to mass spectrometry. Thermogravimetric analysis showed that degradation reactions (devolatilization) initiated at around 180 °C, dropping from approximately 90% to 20% of the samples’ mass. Our work showed that despite presenting a low heating value, both biomass and non-toxic M. aeruginosa LTPNA 01 could be used as energy sources either by burning or producing biofuels. Both can be considered a protein and carbohydrate source similar to some microalgae species as well as biomass fuel. It could also be used as additive for animal feed; however, its safety and potential adverse health effects should be further investigated.

Download Full-text

Evidence of Quorum Sensing in Cyanobacteria by Homoserine Lactones: The Origin of Blooms

Water ◽

10.3390/w13131831 ◽

2021 ◽

Vol 13 (13) ◽

pp. 1831

Author(s):

Natalia Herrera ◽

Fernando Echeverri

Keyword(s):

Cell Proliferation ◽

Quorum Sensing ◽

Microcystis Aeruginosa ◽

Industrial Effluents ◽

Cyanobacterial Blooms ◽

Cylindrospermopsis Raciborskii ◽

Bacterial Communication ◽

Homoserine Lactones ◽

Exogenous Compounds ◽

Almost All

Although several theories have been postulated to explain cyanobacterial blooms, their biochemical origin has not yet been found. In this work, we explore the existence of bacterial communication, called quorum sensing, in Microcystis aeruginosa and Cylindrospermopsis raciborskii. Thus, the application of several known acylhomoserine lactones to cultures of both cyanobacteria causes profound metabolic. At 72 h post-application, some of them produced substantial increases in cell proliferation, while others were inhibitors. There was a correlation with colony-forming activity for most of them. According to ELISA analysis, the microcystin levels were increased with some lactones. However, there was a clear difference between M. aeruginosa and C. raciborskii culture since, in the first one, there was an inducing effect on cell proliferation, while in C. raciborskii, the effects were minor. Besides, there were compound inhibitors and inducers of microcystins production in M. aeruginosa, but almost all compounds were only inducers of saxitoxin production in C. raciborskii. Moreover, each lactone appears to be involved in a specific quorum sensing process. From these results, the formation of cyanobacterial blooms in dams and reservoirs could be explained since lactones may come from cyanobacteria and other sources as bacterial microflora-associated or exogenous compounds structurally unrelated to lactones, such as drugs, industrial effluents, and agrochemicals.

Download Full-text

Terminal Proterozoic cyanobacterial blooms and phosphogenesis documented by the Doushantuo granular phosphorites I: In situ micro-analysis of textures and composition

Precambrian Research ◽

10.1016/j.precamres.2013.05.011 ◽

2013 ◽

Vol 235 ◽

pp. 20-35 ◽

Cited By ~ 37

Author(s):

Zhenbing She ◽

Paul Strother ◽

Gregory McMahon ◽

Larry R. Nittler ◽

Jianhua Wang ◽

...

Keyword(s):

Cyanobacterial Blooms ◽

Micro Analysis

Download Full-text

Predation by three glacial opportunists on natural zooplankton communities

Canadian Journal of Zoology ◽

10.1139/z86-009 ◽

1986 ◽

Vol 64 (1) ◽

pp. 57-64 ◽

Cited By ~ 31

Author(s):

Redwood W. Nero ◽

W. Gary Sprules

Keyword(s):

Previous Survey ◽

Clearance Rates ◽

Mysis Relicta ◽

Chydorus Sphaericus ◽

Theoretical Comparison ◽

Feeding Experiments ◽

Predatory Impact ◽

Limnocalanus Macrurus ◽

Zooplankton Communities

We examine the influence of three glacial opportunist predators, Mysis relicta, Limnocalanus macrurus, and Senecella calanoides, on natural zooplankton communities of central Ontario through a series of feeding experiments in small enclosures (23.6 L). Estimates of in situ clearance rates by M. relicta match previously determined rates, with the following gradation of values: Asplanchna sp. > daphnids and bosminids > Epischura lacustris > large cyclopoids, Chydorus sphaericus and small Diaptomus sp. > L. macrurus > S. calanoides. Clearance rates by M. relicta are similar for all daphnids and bosminids. Hypolimnetic species like Daphnia longiremis and Eubosmina longispina are apparently eliminated by M. relicta, while similarly vulnerable species survive because they have an epilimnetic refuge from M. relicta. Limnocalanus macrurus and S. calanoides prey primarily on copepods, Diaphanosoma spp., and rotifers in the hypolimnion. When both clearance rates and population densities of M. relicta, L. macrurus, and S. calanoides are taken into account, the total predatory impact of M. relicta is much larger than that of the two relict copepods. Based on a theoretical comparison of measured clearance rates by predators with estimated rates of prey recruitment, we conclude that differences in species composition and abundance between relict and nonrelict lakes described in a previous survey are due principally to predation by M. relicta.

Download Full-text

Using a two-layered sphere model to investigate the impact of gas vacuoles on the inherent optical properties of <i>Microcystis aeruginosa</i>

Biogeosciences ◽

10.5194/bg-10-8139-2013 ◽

2013 ◽

Vol 10 (12) ◽

pp. 8139-8157 ◽

Cited By ~ 13

Author(s):

M. W. Matthews ◽

S. Bernard

Keyword(s):

Optical Properties ◽

Microcystis Aeruginosa ◽

Cyanobacterial Blooms ◽

Shell Layer ◽

Sphere Model ◽

Homogeneous Population ◽

Chl A ◽

Inherent Optical Properties ◽

Gas Vacuoles ◽

The Impact

Abstract. A two-layered sphere model is used to investigate the impact of gas vacuoles on the inherent optical properties (IOPs) of the cyanophyte Microcystis aeruginosa. Enclosing a vacuole-like particle within a chromatoplasm shell layer significantly altered spectral scattering and increased backscattering. The two-layered sphere model reproduced features in the spectral attenuation and volume scattering function (VSF) that have previously been attributed to gas vacuoles. This suggests the model is good at least as a first approximation for investigating how gas vacuoles alter the IOPs. Measured Rrs was used to provide a range of values for the central value of the real refractive index, 1 + ε, for the shell layer using measured IOPs and a radiative transfer model. Sufficient optical closure was obtained for 1 + ε between 1.1 and 1.14, which had corresponding Chl a-specific phytoplankton backscattering, bbφ*, between 3.9 and 7.2 × 10−3 m2 mg−1 at 510 nm. The bbφ* values are in close agreement with the literature and in situ particulate backscattering measurements. Rrs simulated for a population of vacuolate cells was greatly enlarged relative to a homogeneous population. A sensitivity analysis of empirical algorithms for estimating Chl a in eutrophic/hypertrophic waters suggests these are robust under variable constituent concentrations and likely to be species-sensitive. The study confirms that gas vacuoles cause significant increase in backscattering and are responsible for the high Rrs values observed in buoyant cyanobacterial blooms. Gas vacuoles are therefore one of the most important bio-optical substructures influencing the IOPs in phytoplankton.

Download Full-text