Grazing rates on toxic and non-toxic strains of cyanobacteria by Hypophthalmichthys molitrix and Oreochromis niloticus

The tilapia Oreochromis niloticus and the silver carp Hypophthalmichthys molitrix were exposed to toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa in order to determine if cells of the toxic strain were ingested and, if not, by what mechanism they were excluded. Enumeration of cyanobacterial particles before and after exposure to fish showed that there were no significant differences (P<0.05) at the end of the trial between the toxic treatment and the control consisting of toxic M. aeruginosa with no fish. Fish exposed to the non-toxic strain increased opercular beat rate, elevating the volumes of water and food material passed over the gills whereas those that were held in the toxic strain did not. Of the cyanobacterial toxins (microcystins) presented to the fish, most were in the cyanobacterial cells, toxin levels in the water being below the level of detectability (<250 ng l⁻¹), The ability of the fish to differentiate between toxic and non-toxic cyanobacterial strains may thus be determined by very low levels of extracellular microcystins or/and other features which distinguish toxic from non-toxic M. aeruginosa strains, such as cell surface components.     

Antialgal activity of a hepatotoxin-producing cyanobacterium,Microcystis aeruginosa

Antimicrobial activity of toxin produced by a freshwater bloom-forming cyanobacterium Microcystis aeruginosa has been studied. When tested against certain green algae, cyanobacteria, heterotrophic bacteria and fungi, the toxin inhibited growth of only green algae and cyanobacteria. The toxin has been partially purified employing Thin layer chromatography (TLC) and High-performance liquid chromatography (HPLC) techniques and appears to be microcystin-LR (leucine–arginine). Both crude and purified toxins showed toxicity to mice, the clinical symptoms in test mice being similar to those produced by hepatotoxin. Purified toxin at a concentration of 50 g ml^–1 caused complete inhibition of growth followed by cell lysis in Nostoc muscorum and Anabaena BT1 after 6 days of toxin addition. Addition of toxin (25 g ml^–1) to the culture suspensions of the Nostoc and Anabaena strains caused instant and drastic loss of O₂ evolution. Furthermore a marked reduction (about 87%) in the ¹⁴CO₂ uptake was also observed at a concentration of 50 g ml^–1. Besides its inhibitory effects on photosynthetic processes, M. aeruginosa toxin (50 g ml^–1) also caused 90% loss of nitrogenase activity after 8 h of its addition. Experiments performed with ¹⁴C-labelled toxin indicate that the toxin uptake by cyanobacterial cells occurs both in light and dark. These results demonstrate that the toxin is strongly algicidal and point to the possibility that it may have an important role in establishment and maintenance of toxic blooms of M. aeruginosa in freshwater ecosystems. The relative significance of the hepatotoxic effect and the algicidal effect of the toxin is discussed with reference both to survival and dominance of M. aeruginosa in nature.     

Isolation and characterization of a cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa

We isolated a cyanophage (Ma-LMM01) that specifically infects a toxic strain of the bloom-forming cyanobacterium Microcystis aeruginosa. Transmission electron microscopy showed that the virion is composed of anisometric head and a tail complex consisting of a central tube and a contractile sheath with helical symmetry. The morphological features and the host specificity suggest that Ma-LMM01 is a member of the cyanomyovirus group. Using semi-one-step growth experiments, the latent period and burst size were estimated to be 6 to 12 h and 50 to 120 infectious units per cell, respectively. The size of the phage genome was estimated to be ca. 160 kbp using pulse-field gel electrophoresis; the nucleic acid was sensitive to DNase I, Bal31, and all 14 restriction enzymes tested, suggesting that it is a linear double-stranded DNA having a low level of methylation. Phylogenetic analyses based on the deduced amino acid sequences of two open reading frames coding for ribonucleotide reductase alpha- and beta-subunits showed that Ma-LMM01 forms a sister group with marine and freshwater cyanobacteria and is apparently distinct from T4-like phages. Phylogenetic analysis of the deduced amino acid sequence of the putative sheath protein showed that Ma-LMM01 does not form a monophyletic group with either the T4-like phages or prophages, suggesting that Ma-LMM01 is distinct from other T4-like phages that have been described despite morphological similarity. The host-phage system which we studied is expected to contribute to our understanding of the ecology of Microcystis blooms and the genetics of cyanophages, and our results suggest the phages could be used to control toxic cyanobacterial blooms.     

Responses of the toxic cyanobacterium Microcystis aeruginosa to iron and humic substances.

Iron is an essential element to marine biota. Different types of dissolved organic matter (DOM), such as humic substances have impacts on the marine coastal waters iron chemistry. The aim of the study was to examine how the presence of humic substances (both aquatic and sedimentary) may affect iron bioavailability to the bloom-forming cyanobacterium Microcystis aeruginosa Kutzing incubated on standard and modified mineral BG-11 media. The final iron concentrations in the growth media ranged from 0.1 to 100microM. The results demonstrate that both the growth rate and the concentration of chlorophyll a in cultures of M. aeruginosa are limited by insufficient (<10microM) Fe concentrations. The addition of aquatic humic substances in the presence of iron in concentrations <0.1microM increased the optical density 25-fold, and the production of chlorophyll a 15-fold as compared with the cultures exposed to iron only at the same concentration. Sedimentary humic acids in the presence of iron at a concentration of 10microM reduced the growth and production of chlorophyll a by 50% as compared to the cultures exposed to iron only at the same concentration. Possible mechanisms of humic substances - metal ion - alga interactions are discussed. It is suggested that aquatic humic substances could be of great importance in the formation of cyanobacteria blooms.     

Photoinactivation in vivo of superoxide dismutase and catalase in the cyanobacterium Microcystis aeruginosa

Abstract The planktonic cyanobacterium Microcystis aeruginosa is particularly sensitive to photoinhibition by visible light, Photosystem II and ribulose 1,5-bisphosphate (RuBP) carboxylase activities being affected. Although the organism contains superoxide dismutase (SOD) and catalase, these protective enzymes are also photoinactivated during the illumination of whole cells by visible light.     

Activity of some Nile River aquatic macrophyte extracts against the cyanobacterium Microcystis aeruginosa

The anti-algal activity of five macrophyte extracts on the cyanobacterium Microcystis aeruginosa in Egypt was investigated in 2013. Extract activity varied according to plant type, extracting solvent and its concentration. The highest inhibitory activity was achieved with ethanol extract at a concentration of 80 mg l^?1, followed by chloroformic extracts, at 60 mg l^?1. Methanolic extracts of Eichhornia crassipes and Polygonum tomentosum inhibited growth of Microcystis aeruginosa at all concentrations. Acetonic extracts inhibited algal growth at 60 mg l^?1, except for the extract of Ceratophyllum subdemersum, which showed stimulation of M. aeruginosa growth. Eichhornia crassipes ethanolic extract exerted the most powerful inhibition by more than five-fold, 570.17%, followed by those of P. tomentosum, Saccharum spontaneum, Ceratophyllum demersum and C. subdemersum, 559.48, 553.99, 544.11 and 366.51%, respectively. Phytochemical screening for the tested plant extracts revealed the presence of biologically active substances of different concentrations, with P. tomentosum having the highest polyphenols, 1.95% of dry weight.     

Growth inhibition of bloom-forming cyanobacterium Microcystis aeruginosa by rice straw extract

AIMS: To inhibit the growth of the bloom-forming cyanobacterium Microcystis aeruginosa using a rice straw extract. METHODS AND RESULTS: The cell numbers of the algal strain M. aeruginosa UTEX 2388 significantly decreased after treatment with different concentrations (0.01, 0.1, 1 and 10 mg l(-1)) of a rice straw extract for an 8-day cultivation period. Among seven tested allelochemicals from rice straw, salicylic acid at 0.1 mg l(1) exhibited the highest allelopathic activity (26%) on day 8. A synergistic effect on algal growth inhibition was found when adding two or three phenolic compounds from the rice straw. CONCLUSIONS: The growth of M. aeruginosa was inhibited by rice straw extract concentrations ranging from 0.01 to 10 mg l(1). This activity was due to the synergistic effects of various phenolic compounds in the rice straw. SIGNIFICANCE AND IMPACT OF THE STUDY: The identification of rice straw as an effective material for the growth inhibition of M. aeruginosa implies it may have the potential to be used as an environment-friendly biomaterial for controlling the algal bloom of M. aeruginosa in eutrophic water.     

Functional analysis of PilT from the toxic cyanobacterium Microcystis aeruginosa PCC 7806

The evolution of the microcystin toxin gene cluster in phylogenetically distant cyanobacteria has been attributed to recombination, inactivation, and deletion events, although gene transfer may also be involved. Since the microcystin-producing Microcystis aeruginosa PCC 7806 is naturally transformable, we have initiated the characterization of its type IV pilus system, involved in DNA uptake in many bacteria, to provide a physiological focus for the influence of gene transfer in microcystin evolution. The type IV pilus genes pilA, pilB, pilC, and pilT were shown to be expressed in M. aeruginosa PCC 7806. The purified PilT protein yielded a maximal ATPase activity of 37.5 +/- 1.8 nmol P(i) min(-1) mg protein(-1), with a requirement for Mg(2+). Heterologous expression indicated that it could complement the pilT mutant of Pseudomonas aeruginosa, but not that of the cyanobacterium Synechocystis sp. strain PCC 6803, which was unexpected. Differences in two critical residues between the M. aeruginosa PCC 7806 PilT (7806 PilT) and the Synechocystis sp. strain PCC 6803 PilT proteins affected their theoretical structural models, which may explain the nonfunctionality of 7806 PilT in its cyanobacterial counterpart. Screening of the pilT gene in toxic and nontoxic strains of Microcystis was also performed.     

Size‐structured vulnerability of the colonial cyanobacterium,Microcystis aeruginosa,to grazing by zebra mussels (Dreissena polymorpha)

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The effect of pre-industrial and predicted atmospheric CO2 concentrations on the development of diazotrophic and non-diazotrophic cyanobacterium: Dolichospermum circinale and Microcystis aeruginosa

Photoautotrophs are capable of consuming high quantities of CO₂, yet scant research exists examining the influence of different CO₂ concentrations on the growth of freshwater diazotrophic or non-diazotrophic cyanobacteria. In this study, we cultured two cyanobacteria taxa (Dolichospermum circinale and Microcystis aeruginosa) within controlled atmospheric CO₂ chambers at pre-industrial, and post-industrial concentrations. Biovolume and chlorophyll a (Chl-a) differed as a consequence of the adjusted CO₂ gradients. Significantly higher biovolume measurements were observed in the elevated CO₂ treatment for the diazotrophic species in the initial experiment. However, a follow-up experiment, with a corrected culture replenishment regime showed Chl-a measurements were greater for the diazotrophic and non-diazotrophic species in the elevated CO₂ treatment. Increasing CO₂ presents a risk to already compromised eutrophic and hyper-eutrophic ecosystems, and we reason increasing CO₂ concentrations could affect photosynthetic performance and CO₂ assimilation of surface dwelling cyanobacteria. Further experimental work is required to establish ecological thresholds for freshwater ecosystems, as pH levels showed a measurable reduction within the elevated CO₂ treatments. As cyanobacteria species may respond quite differently to future CO₂ concentrations similar comparative studies should be carried out that focus on CO₂ dynamics and pH. The findings of the study indicate diazotrophic cyanobacteria growth in particular may benefit from elevated atmospheric CO₂ concentrations.     

Ecological dynamics of the toxic bloom-forming cyanobacterium Microcystis aeruginosa and its cyanophages in freshwater

The abundance of potentially Microcystis aeruginosa-infectious cyanophages in freshwater was studied using g91 real-time PCR. A clear increase in cyanophage abundance was observed when M. aeruginosa numbers declined, showing that these factors were significantly negatively correlated. Furthermore, our data suggested that cyanophage dynamics may also affect shifts in microcystin-producing and non-microcystin-producing populations.     

Growth and photosynthetic response of the cyanobacterium Microcystis aeruginosa in relation to photoperiodicity and irradiance

Growth and photosynthetic characteristics, P _max (maximum light-saturated oxygen production rate) and (photosynthetic affinity), of Microcystis aeruginosa were studied in continuous cultures under a range of photoperiod lengths and growth irradiances. Microcystis showed a low specific maintenance rate constant and a high growth affinity for light (typical cyanobacterial features), but required a dark period to obtain maximum growth rate. P _max and per unit dry weight increased, as did pigment content, when less light became available. By regulation in and P _max (crucial in light-limiting and high-light conditions, respectively) this buoyant species can flourish in low light, but also in high-light environments which may arise when buoyancy is lost.The two different types of light conditions affected growth, and photosynthesis, in different ways. One needs thus to discriminate between photoperiod- and irradiance-limitation, which restricts the utility of simple algal growth models. It was emphasized that photosynthetic adaptation patterns of light-limited species may resemble short-term nutrient uptake kinetics of nutrient-limited organisms.With prior knowledge of the growth limitation, we were able to assess the growth rate of a natural population of Microcystis from its photosynthetic response and from data of laboratory cultures of a known physiological state.     

Somatic and population growth in selected cladoceran and rotifer species offered the cyanobacterium it Microcystis aeruginosa as food

The ability of cladocerans and rotifers to utilise the cyanobacterium Microcystis aeruginosa was tested by comparing the somatic and population growth in cultures using Chlorella and Microcystis as food types. Five species of cladocerans (Ceriodaphnia cornuta, Scapholeberis kingi, Moina macrocopa, Daphnia carinata, Simocephalus vetulus) and two species of rotifers (Brachionus calyciflorus, Hexarthra mira) were used in this study. In order to exclude the possibility of poor utilisation of Microcystis due to mechanical interference, single cells of Microcystis, (obtained by sonicating large colonies) were also offered. Experiments were done at 20 °Cs and 30 °C . In all the treatments tested, the population growth rate per day of the cladocerans ranged from -0.715 to 0.612 and that of the rotifers from -1.15 to 0.781. While C. cornuta, S. kingi and S. vetulus could utilise Microcystis, M. macrocopa and D. carinata were extremely susceptible to its toxins. The ability of the cladoceran populations to grow on Microcystis single cells was not related to the body length or gut length alone but to their ratio. The toxic effects of Microcystis were mitigated at the higher temperature. A strain of C. cornuta, collected from a Microcystis-dominated lake, had a higher growth rate on the toxic cyanobacteria suggesting that the tolerance to Microcystis could be a heritable trait. Of the two rotifer species, only H. mira survived and reproduced in some treatments of Microcystis. This revised version was published online in July 2006 with corrections to the Cover Date.     

Growth of a grazing phytoplanktivorous fish and growth enhancement of the grazed alga

Summary The blue tilapia, Tilapia aurea, consumes the green alga, Ankistrodesmus falcatus, with some algal cells passing through the gut in viable condition. Grazing fish grew and the grazed algal populations had enhanced densities compared to ungrazed populations. Algal growth enhancement was not produced by either bacteria or fish excreting an algal limiting nutrient. Possible ingestion and digestion of bacterial cells by the fish might release nutrients to the algal cells that were otherwise unavailable. Blue tilapia may be affecting algal communities in ways other than by passive size selection. Enhancement of algal growth by the blue tilapia could have important implications for understanding the phytoplankton dynamics in waters containing blue tilapia.     

Foraging strategies and growth inhibition in five daphnids feeding on mixtures of a toxic cyanobacterium and a green alga

1. Laboratory experiments were used to study the feeding, growth and reproduction of five daphnids in mixtures of a toxic cyanobacterium, Microcystis aeruginosa, and a green alga, Scenedesmus acutus. The mixtures included 0%, 20%, 50%, 80% and 100% Microcystis with a total food concentration of 0.5 mg C L^??1 in each treatment. The feeding rate was measured after 1 and 24 h of acclimatization to the mixtures. 2. Toxic Microcystis inhibited feeding in all the species, but they exhibited an unexpected diversity and complexity in the pattern of feeding inhibition. Daphnia magna exhibited the strongest inhibition of feeding after 1 h of exposure to toxic food, but had substantially recovered after 24 h in the same mixtures. This pattern of inhibition and recovery may balance the benefits of reduced ingestion of toxin with the disadvantage of a reduced energy intake. 3. All five daphnids grew quickly in the Scenedesmus control, whereas growth and reproduction declined with an increasing proportion of the toxic alga in the diet. Daphnia pulicaria showed the least inhibition of growth and reproduction, D. pulex showed the strongest inhibition and the three remaining species exhibited intermediate sensitivity. 4. Estimates of gross growth efficiency (GGE; growth/ingestion) provided a means for discriminating between the effects of feeding inhibition and direct toxicity on zooplankton growth. Daphnia pulex exhibited a sharp decline in GGE, suggesting that growth inhibition was a result of both feeding inhibition and direct toxicity. In contrast, D. magna exhibited a nearly constant GGE, indicating that feeding inhibition accounted for its decline in growth. However, two Daphnia species (i.e. D. pulicaria and D. galeata) exhibited improbable increases in GGE with toxic cyanobacteria, suggesting that their feeding rates were underestimated. Growth assays with sensitive and resistant zooplankton species are proposed for testing the potential impacts toxic cyanobacteria in lakes.     

Maternal consumption of non‐toxic Microcystis by Daphnia magna induces tolerance to toxic Microcystis in offspring

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Adaptation of the toxic freshwater cyanobacterium Microcystis aeruginosa to salinity is achieved by the selection of spontaneous mutants

The cyanobacterium Microcystis aeruginosa causes most of the harmful toxic blooms in freshwater ecosystems. Some strains of M. aeruginosa tolerate low‐medium levels of salinity, and because salinization of freshwater aquatic systems is increasing worldwide it is relevant to know what adaptive mechanisms allow tolerance to salinity. The mechanisms involved in the adaptation of M. aeruginosa to salinity (acclimation vs. genetic adaptation) were tested by a fluctuation analysis design, and then the maximum capacity of adaptation to salinity was studied by a ratchet protocol experiment. Whereas a dose of 10 g NaCl L^?1 completely inhibited the growth of M. aeruginosa, salinity‐resistant genetic variants, capable of tolerating up to 14 g NaCl L^?1, were isolated in the fluctuation analysis experiment. The salinity‐resistant cells arose by spontaneous mutations at a rate of 7.3 × 10^?7 mutants per cell division. We observed with the ratchet protocol that three independent culture populations of M. aeruginosa were able to adapt to up to 15.1 g L^?1 of NaCl, suggesting that successive mutation‐selection processes can enhance the highest salinity level to which M. aeruginosa cells can initially adapt. We propose that increasing salinity in water reservoirs could lead to the selection of salinity‐resistant mutants of M. aeruginosa.     

Predictability and possible mechanisms of plankton response to reduction of planktivorous fish

The predictability of plankton response to reductions of planktivorous fish was investigated by comparing the plankton community in three biomanipulated lakes and ten unmanipulated lakes differing in intensity of fish predation. Data collected on total phosphorus, phytoplankton and zooplankton biomass and share of cyanobacteria and large grazers, as well as specific growth rate of phytoplankton, were further used to test some of the proposed underlying response-mechanisms. In the biomanipulated lakes the algal biomass and share of cyanobacteria decreased, specific growth rate of phytoplankton increased, and zooplankton biomass and share of large grazers increased or remained unchanged. This pattern was largely reflected in the differences in food-chain structure between the unmanipulated lakes with highversus those with low fish predation. The qualitative response to planktivorous fish reduction thus seems largely predictable. The biomanipulated lakes differed, however, in magnitude of response: the smallest hypertrophic, rotenone-treated lake (Helgetjern) showed the most dramatic response, whereas the large, deep mesotrophic lake (Gjersjøen), which was stocked with piscivorous fish, showed more moderate response, probably approaching a new steady state. These differences in response magnitude may be related to different perturbation intensity (rotenone-treatmentversus stocking with piscivores), food-chain complexity and trophic state. Both decreased phosphorus concentration and increased zooplankton grazing are probably important mechanisms underlying plankton response to biomanipulation in many lakes. The results provide tentative support to the hypothesis that under conditions of phosphorus limitation, increased zooplankton grazing can decrease algal biomassvia two separate mechanisms: reduction of the phosphorus pool in the phytoplankton, and reduction of the internal C:P-ratio in the phytoplankton cells.

     

Cryopreservation of a water-bloom forming cyanobacterium, Microcystis aeruginosa f. aeruginosa

A method for the Cryopreservation of Microcystis aeruginosa f. aeruginosa is described. For the five strains tested, dimethyl sulfoxide (DMSO) (3% v/v) was the only effective cryoprotectant for freezing to, and thawing from -196°C and allowed the successful recovery (>50%) of all the strains. The viability of frozen material was independent of the period of storage in liquid nitrogen. The strain NIES-44 (National Institute for Environmental Studies) had a recovery level of greater than 90% at 3–10% (v/v) DMSO in both two step and rapid cooling methods. The other three strains, NIES-87, 88 and 89 had greater than 60% of viability after freeze/thawing in presence of both 3% and 5% DMSO concentrations. On the other hand, the strain NIES-90 showed approximately 50% of viability in only 3% DMSO solution after two step cooling to and thawing from -196°C. This strain was damaged by greater than 4% DMSO and by rapid cooling to -196°C. It was found that cold shock injury and the cytotoxicity of DMSO were different at a strain level.     

The effects of the cyanobacterium Microcystis aeruginosa, the cyanobacterial hepatotoxin microcystin–LR, and ammonia on growth rate and ionic regulation of brown trout

Brown trout were exposed for 63 days to five treatments: a control; the purified cyanobacterial hepatotoxin microcystin—LR (MC—LR) (41—57 μg MC—LR 1^?1); lysed toxic Microcystis aeruginosa cells (41–68 μg MC—LR 1^?1 and 288 μg chlorophyll a 1^?1); lysed non—toxic M. aeruginosa cells (non—MC—LR containing and 288 μg chlorophyll a 1^?1); ammonia (65–325 μg NH₃ 1^?1). All treatments produced significantly reduced growth compared to controls (P<0·05, Fisher test). Exposure to ammonia resulted weight loss over the first 7 days followed by weight increase, though at a significantly lower level than in the other treatments. First exposed to lysed toxic M. aeruginosa cells grew less than those exposed to lysed non—toxic cyanobacteria or purified MC—LR. Sodium influx rates after 63 days exposure to purified MC—LR, lysed toxic M. aeruginosa cells, or ammonia showed a significant increase compared to control fish or those exposed to lysed non—toxic M. aeruginosa cells. There were no significant differences in Na⁺ efflux or net Na⁺ uptake rates between treatments. Significant increases in body Na⁺ and Cl^— were seen in fish exposed to lysed toxic M. aeruginosa cells or ammonia. Only fish exposed to ammonia showed a significant increase in body ammonia. Short—term exposure, over 4 h, to lysed toxic cells, non—toxic cells or purified MC—LR resulted in insignificant changes in Na⁺ flux rates compared to controls although there was a significant net Na⁺ loss in fish exposed to ammonia. Chronic exposure of fish to toxic cyanobacterial blooms may result in ionic imbalance and reduced growth.