Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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State transitions in the cyanobacterium Synechococcus elongatus 7942 involve reversible quenching of the photosystem II core
Ranjbar Choubeh, Reza ; Wientjes, Emilie ; Struik, Paul C. ; Kirilovsky, Diana ; Amerongen, Herbert van - \ 2018
Biochimica et Biophysica Acta. B, Bioenergetics 1859 (2018)10. - ISSN 0005-2728 - p. 1059 - 1066.
Cyanobacteria - Photosystem II - State transitions - Time-resolved fluorescence spectroscopy

Cyanobacteria use chlorophyll and phycobiliproteins to harvest light. The resulting excitation energy is delivered to reaction centers (RCs), where photochemistry starts. The relative amounts of excitation energy arriving at the RCs of photosystem I (PSI) and II (PSII) depend on the spectral composition of the light. To balance the excitations in both photosystems, cyanobacteria perform state transitions to equilibrate the excitation energy. They go to state I if PSI is preferentially excited, for example after illumination with blue light (light I), and to state II after illumination with green-orange light (light II) or after dark adaptation. In this study, we performed 77-K time-resolved fluorescence spectroscopy on wild-type Synechococcus elongatus 7942 cells to measure how state transitions affect excitation energy transfer to PSI and PSII in different light conditions and to test the various models that have been proposed in literature. The time-resolved spectra show that the PSII core is quenched in state II and that this is not due to a change in excitation energy transfer from PSII to PSI (spill-over), either direct or indirect via phycobilisomes.

Effects of temperature, genetic variation and species competition on the sensitivity of algae populations to the antibiotic enrofloxacin
Rico, Andreu ; Zhao, Wenkai ; Gillissen, Frits ; Lürling, Miquel ; Brink, Paul J. van den - \ 2018
Ecotoxicology and Environmental Safety 148 (2018). - ISSN 0147-6513 - p. 228 - 236.
Antibiotics - Cyanobacteria - Green algae - Species competition - Temperature-dependent sensitivity

Primary producers are amongst the most sensitive organisms to antibiotic pollution in aquatic ecosystems. To date, there is little information on how different environmental conditions may affect their sensitivity to antibiotics. In this study we assessed how temperature, genetic variation and species competition may affect the sensitivity of the cyanobacterium Microcystis aeruginosa and the green-algae Scenedesmus obliquus to the antibiotic enrofloxacin. First, we performed single-species tests to assess the toxicity of enrofloxacin under different temperature conditions (20 °C and 30 °C) and to assess the sensitivity of different species strains using a standard temperature (20 °C). Next, we investigated how enrofloxacin contamination may affect the competition between M. aeruginosa and S. obliquus. A competition experiment was performed following a full factorial design with different competition treatments, defined as density ratios (i.e. initial bio-volume of 25/75%, 10/90% and 1/99% of S. obliquus/M. aeruginosa, respectively), one 100% S. obliquus treatment and one 100% M. aeruginosa treatment, and four different enrofloxacin concentrations (i.e. control, 0.01, 0.05 and 0.10 mg/L). Growth inhibition based on cell number, bio-volume, chlorophyll-a concentration as well as photosynthetic activity were used as evaluation endpoints in the single-species tests, while growth inhibition based on measured chlorophyll-a was primarily used in the competition experiment. M. aeruginosa photosynthetic activity was found to be the most sensitive endpoint to enrofloxacin (EC50–72 h =0.02 mg/L), followed by growth inhibition based on cell number. S. obliquus was found to be slightly more sensitive at 20 °C than at 30 °C (EC50–72 h cell number growth inhibition of 38 and 41 mg/L, respectively), whereas an opposite trend was observed for M. aeruginosa (0.047 and 0.037 mg/L, respectively). Differences in EC50–72 h values between algal strains of the same species were within a factor of two. The competition experiment showed that M. aeruginosa growth can be significantly reduced in the presence of S. obliquus at a density ratio of 75/25% M. aeruginosa/S. obliquus, showing a higher susceptibility to enrofloxacin than in the single-species test. The results of this study confirm the high sensitivity of cyanobacteria to antibiotics and show that temperature and inter-strain genetic variation may have a limited influence on their response to them. The results of the competition experiment suggest that the structure of primary producer communities can be affected, at least temporarily, at antibiotic concentrations close to those that have been measured in the environment.

Picosecond excitation energy transfer of allophycocyanin studied in solution and in crystals
Ranjbar Choubeh, Reza ; Sonani, Ravi R. ; Madamwar, Datta ; Struik, Paul C. ; Bader, Arjen N. ; Robert, Bruno ; Amerongen, Herbert van - \ 2018
Photosynthesis Research 135 (2018)1-3. - ISSN 0166-8595 - p. 79 - 86.
Allophycocyanin crystals - Cyanobacteria - Excitation energy transfer - Phycobilisome - Time-resolved fluorescence spectroscopy

Cyanobacteria perform photosynthesis with the use of large light-harvesting antennae called phycobilisomes (PBSs). These hemispherical PBSs contain hundreds of open-chain tetrapyrrole chromophores bound to different peptides, providing an arrangement in which excitation energy is funnelled towards the PBS core from where it can be transferred to photosystem I and/or photosystem II. In the PBS core, many allophycocyanin (APC) trimers are present, red-light-absorbing phycobiliproteins that covalently bind phycocyanobilin (PCB) chromophores. APC trimers were amongst the first light-harvesting complexes to be crystallized. APC trimers have two spectrally different PCBs per monomer, a high- and a low-energy pigment. The crystal structure of the APC trimer reveals the close distance (~21 Å) between those two chromophores (the distance within one monomer is ~51 Å) and this explains the ultrafast (~1 ps) excitation energy transfer (EET) between them. Both chromophores adopt a somewhat different structure, which is held responsible for their spectral difference. Here we used spectrally resolved picosecond fluorescence to study EET in these APC trimers both in crystallized and in solubilized form. We found that not all closely spaced pigment couples consist of a low- and a high-energy pigment. In ~10% of the cases, a couple consists of two high-energy pigments. EET to a low-energy pigment, which can spectrally be resolved, occurs on a time scale of tens of picoseconds. This transfer turns out to be three times faster in the crystal than in the solution. The spectral characteristics and the time scale of this transfer component are similar to what have been observed in the whole cells of Synechocystis sp. PCC 6803, for which it was ascribed to EET from C-phycocyanin to APC. The present results thus demonstrate that part of this transfer should probably also be ascribed to EET within APC trimers.

Effect of suspended clay on growth rates of the cyanobacterium Cylindrospermopsis raciborskii
Brasil, Jandeson ; Huszar, Vera L.M. ; Attayde, José L. ; Marinho, Marcelo M. ; Oosterhout, Frank Van; Lürling, Miquel - \ 2017
Fundamental and Applied Limnology 191 (2017)1. - ISSN 1863-9135 - p. 13 - 23.
Cyanobacteria - Inorganic turbidity - Light availability - Sedimentation - Suspended solids
Recent studies have shown that sediment resuspension may lead to the collapse of C. raciborskii dominance, which suggests that clay might have a negative effect on the growth of C. raciborskii. To test the hypothesis that suspended clay creates an unfavorable environment for growth of C. raciborskii, we exposed four different strains of this species to various concentrations of the clays kaolinite and bentonite, and monitored the biomass of each strain over the course of 1-week microcosm experiments. Contrary to our hypothesis, C. raciborskii was able to grow in suspensions of both clays. While kaolinite clay caused higher turbidity than bentonite, the growth rates of all four C. raciborskii strains were higher in kaolinite than in bentonite suspensions. C. raciborskii could still grow in clay concentrations that cause turbidity far above the levels found in natural lakes. Our study suggests that the reported collapse of C. raciborskii blooms with high concentrations of suspended sediments in tropical shallow lakes is probably not caused by the effects of suspended clay on light attenuation, but rather is a consequence of cell sinking or, possibly a response to disturbance events responsible for sediment suspension.
Bio-accumulation of lanthanum from lanthanum modified bentonite treatments in lake restoration
Waajen, G. ; Oosterhout, F. van; Lürling, M. - \ 2017
Environmental Pollution 230 (2017). - ISSN 0269-7491 - p. 911 - 918.
Cyanobacteria - Ecotoxicity - Eutrophication control - Health risk - Phoslock
Lanthanum (La) modified bentonite (LMB) is one of the available mitigating agents used for the reduction of the phosphorus (P) recycling in eutrophic lakes. The potential toxicity of the La from LMB to aquatic organisms is a matter of concern. In this study the accumulation of La was investigated in the macrophyte Elodea nuttallii, in chironomid larvae and in several fish species during periods up to five years following in situ LMB applications. The application of LMB increased the La concentration of exposed plants and animals. During the first growing season following LMB applications, the La content of E. nuttallii increased 78 fold (3.98–310.68 μg La g−1 DW) to 127 fold (2.46–311.44 μg La g−1). During the second growing season following application, the La content decreased but was still raised compared to plants that had not been exposed. The La content of chironomids was doubled in the two years following LMB application, although the increase was not significant. Raised La concentrations in fish liver, bone, muscle and skin were observed two and five years following to LMB application. Liver tissues showed the highest La increase, ranging from 6 fold (0.046–0.285 μg La g−1 DW) to ∼20 fold (0.080–1.886 μg La g−1, and 0.122–2.109 μg La g−1) two years following application and from 6 fold (0.046–0.262 μg La g−1) to 13 fold (0.013–0.167 μg La g−1) after five years in pelagic and littoral fish. The La content of the liver from Anguilla anguilla (eel) had increased 94 fold (0.034–3.176 μg La g−1) two years and 133 fold (0.034–4.538 μg La g−1) five years following LMB application. No acute and chronic effects of La accumulation were observed and human health risks are considered negligible. We advocate the long-term study of effects of La accumulation following future LMB applications.
Effects of combined flocculant – Lanthanum modified bentonite treatment on aquatic macroinvertebrate fauna
Waajen, G. ; Pauwels, M. ; Lürling, M. - \ 2017
Water Research 122 (2017). - ISSN 0043-1354 - p. 183 - 193.
Cyanobacteria - Iron-III-chloride - Lake restoration - Macrofauna - Phoslock
A low dose flocculant (FeCl3), combined with lanthanum modified bentonite (LMB) as phosphate-binding agent, has been applied for eutrophication management in Lake De Kuil (The Netherlands). After the treatment, the state of the lake shifted from hypertrophic to mesotrophic. Although macroinvertebrate fauna is important for lake ecosystems, the knowledge of its response to this lake restoration method is fragmented and scarce. Because insight in the macroinvertebrate fauna response is important to assess future applications, pre and post application macroinvertebrate assemblages were identified in Lake De Kuil. The research was accompanied by a microcosm experiment in which the effects of LMB, FeCl3 and LMB + FeCl3 were studied on macroinvertebrate communities. Results show the reduction of macroinvertebrate numbers and taxa during the first month following the application. The number of Gastropoda was strikingly reduced one month after the application. One year after the application, the macroinvertebrate numbers and taxa exceeded the pre-application situation and Gastropoda and Oligochaeta prospered. The effects one month after the treatment are most likely due to the combination of physical impacts of the use of bentonite and chemical impacts of the use of FeCl3, while effects after one year are likely attributed to the shift in trophic state of the lake.
Efficacy of Coagulants and Ballast Compounds in Removal of Cyanobacteria (Microcystis) from Water of the Tropical Lagoon Jacarepaguá (Rio de Janeiro, Brazil)
Magalhães, Leonardo de; Noyma, Natália Pessoa ; Furtado, Luciana Lima ; Nunes Teixeira Mucci, Maira ; Oosterhout, Frank van; Huszar, Vera L.M. ; Marinho, Marcelo Manzi ; Lurling, Miguel - \ 2017
Estuaries and coasts 40 (2017)1. - ISSN 1559-2723 - p. 121 - 133.
Bloom control - Chitosan - Cyanobacteria - Eutrophication - Mitigation - PAC

Eutrophication is considered the most important water quality problem in freshwaters and coastal waters worldwide promoting frequent occurrence of blooms of potentially toxic cyanobacteria. Removal of cyanobacteria from the water column using a combination of coagulant and ballast is a promising technique for mitigation and an alternative to the use of algaecides. In laboratory, we tested experimentally the efficiency of two coagulants, polyaluminium chloride (PAC) and chitosan (made of shrimp shells), alone and combined with two ballasts: red soil (RS) and the own lagoon sediment, to remove natural populations of cyanobacteria, from an urban brackish coastal lagoon. PAC was a very effective coagulant when applied at low doses (≤8 mg Al L−1) and settled the cyanobacteria, while at high doses (≥16 mg Al L−1) large flocks aggregated in the top of test tubes. In contrast, chitosan was not able to form flocks, even in high doses (>16 mg L−1) and did not efficiently settle down cyanobacteria when combined with ballast. The RS itself removed 33–47 % of the cyanobacteria. This removal was strongly enhanced when combined with PAC in a dose-dependent matter; 8 mg Al L−1 was considered the best dose to be applied. The lagoon sediment alone did not promote any settling of cyanobacteria but removal was high when combined with PAC. Combined coagulant and ballast seems a very efficient, cheap, fast and safe curative measure to lessen the harmful cyanobacteria bloom nuisance in periods when particularly needed, such as around the 2016 Olympics in Jacarepaguá Lagoon.

Toxicity Overrides Morphology on Cylindrospermopsis raciborskii Grazing Resistance to the Calanoid Copepod Eudiaptomus gracilis
Machado Rangel, Luciana ; Ger, Kemal A. ; Silva, Lúcia H.S. ; Soares, Maria Carolina S. ; Faassen, Els ; Lurling, Miguel - \ 2016
Microbial Ecology (2016). - ISSN 0095-3628 - p. 835 - 844.
Cyanobacteria - Feeding inhibition - Harmful algal blooms - Saxitoxins - Temperature - Zooplankton

Toxicity and morphology may function as defense mechanisms of bloom-forming cyanobacteria against zooplankton grazing. Yet, the relative importance of each of these factors and their plasticity remains poorly known. We tested the effects of chemical and morphological traits of the bloom-forming cyanobacterium Cylindrospermopsis raciborskii on the feeding response of the selective feeder Eudiaptomus gracilis (Calanoida, Copepoda), using a saxitoxin-producing strain (STX+) and a non-saxitoxin (STX−)-producing strain as food. From these two chemotypes, we established cultures of three different morphotypes that differed in filament length (short, medium, and long) by incubating the strains at 17, 25, and 32 °C. We hypothesized that the inhibitory effects of saxitoxins determine the avoidance of C. raciborskii, and that morphology would only become relevant in the absence of saxitoxins. Temperature affected two traits: higher temperature resulted in significantly shorter filaments in both strains and led to much higher toxin contents in the STX+ strain (1.7 μg eq STX L−1 at 17 °C, 7.9 μg eq STX L−1 at 25 °C, and 25.1 μg eq STX L−1 at 32 °C). Copepods strongly reduced the ingestion of the STX+ strain in comparison with STX− cultures, regardless of filament length. Conversely, consumption of shorter filaments was significantly higher in the STX− strain. The great plasticity of morphological and chemical traits of C. raciborskii and their resultant contrasting effects on the feeding behavior of zooplankton might explain the success of this cyanobacterium in a variety of aquatic environments.

Further improvements in water quality of the Dutch Borderlakes : two types of clear states at different nutrient levels
Noordhuis, Ruurd ; Zuidam, B.G. van; Peeters, E.T.H.M. ; Geest, G.J. van - \ 2016
Aquatic Ecology 50 (2016)3. - ISSN 1386-2588 - p. 521 - 539.
Abramis brama - Alternative stable states - Biomanipulation - Cyanobacteria - Dreissena - Macro-algae - Quagga Mussel - Regime shift - randmeren - mussels - algae - water quality - aquatic ecology - eutrophication - abramis brama - mossels - cyanobacteriën - algen - waterkwaliteit - aquatische ecologie - eutrofiëring

The Borderlakes are a chain of ten shallow, largely artificial, interconnected lakes in the Netherlands. The ecological recovery of the central Borderlakes (viz. lake Veluwe and Wolderwijd) has been well documented. These lakes shifted from a eutrophic, Planktothrix dominated state in the 1970s to a clear state in 1996. Around 2010, the formerly hypertrophic, southern Borderlake Eem also reached a clear state, but at considerably higher nutrient levels. In this paper, monitoring data are used to compare these changes and identify the differences in driving processes and their consequences. The 1996 shift in Lake Veluwe was linked to increased fishery for benthivorous Bream, followed and stabilized by increase in Zebra Mussels and charophytes. Nutrients in Lake Eem decreased as well and Planktothrix disappeared here too in 1996, despite relatively high TP concentrations which remained stable over time. The start of the change into the clear state in this case also involved a decrease in the Bream population, but with a stronger additional role for dreissenids, particularly of Quagga Mussels. Remaining blooms of cyanobacteria almost disappeared, but the current situation in Lake Eem represents a different type of clear water state than in the central Borderlakes. This type is characterized by the combination of a relatively high phosphorus load, intense dreissenid filtration and filamentous macro-algae instead of either blooms of cyanobacteria or dominance of charophytes. With the dominant role of the River Eem, the relatively short residence time and increasing difficulty to bring down nutrient loading any further, the stability of this clear state depends on high densities (and filtration rates) of dreissenids.

GLOBIO-Aquatic, a global model of human impact on the biodiversity of inland aquatic ecosystems
Janse, J.H. ; Kuiper, J.J. ; Weijters, M.J. ; Westerbeek, E.P. ; Jeuken, M.H.J.L. ; Bakkenes, M. ; Alkemade, R. ; Mooij, W.M. ; Verhoeven, J.T.A. - \ 2015
Environmental Science & Policy 48 (2015). - ISSN 1462-9011 - p. 99 - 114.
Catchment - Cyanobacteria - Eutrophication - Hydrological disturbance - Lakes - Land use change - Rivers - Scenario analysis - Wetlands

Biodiversity in freshwater ecosystems - rivers, lakes and wetlands - is undergoing rapid global decline. Major drivers are land use change, eutrophication, hydrological disturbance, climate change, overexploitation and invasive species. We developed a global model for assessing the dominant human impacts on inland aquatic biodiversity. The system consists of a biodiversity model, named GLOBIO-Aquatic, that is embedded in the IMAGE model framework, i.e. linked to models for demography, economy, land use changes, climate change, nutrient emissions, a global hydrological model and a global map of water bodies. The biodiversity model is based on a recompilation of existing data, thereby scaling-up from local/regional case-studies to global trends. We compared species composition in impacted lakes, rivers and wetlands to that in comparable undisturbed systems. We focussed on broad categories of human-induced pressures that are relevant at the global scale. The drivers currently included are catchment land use changes and nutrient loading affecting water quality, and hydrological disturbance and climate change affecting water quantity. The resulting relative mean abundance of original species is used as indicator for biodiversity intactness. For lakes, we used dominance of harmful algal blooms as an additional indicator. The results show that there is a significant negative relation between biodiversity intactness and these stressors in all types of freshwater ecosystems. In heavily used catchments, standing water bodies would lose about 80% of their biodiversity intactness and running waters about 70%, while severe hydrological disturbance would result in losses of about 80% in running waters and more than 50% in floodplain wetlands. As an illustration, an analysis using the OECD 'baseline scenario' shows a considerable decline of the biodiversity intactness in still existing water bodies in 2000, especially in temperate and subtropical regions, and a further decline especially in tropical regions in 2050. Historical loss of wetland areas is not yet included in these results. The model may inform policy makers at the global level in what regions aquatic biodiversity will be affected most and by what causes, and allows for scenario analysis to evaluate policy options.

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