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The Phenomenon of Toxin-Producing Cyanobacterial Blooms and Their Impact on Aquatic Organisms, Ecosystems, and Human Health

A special issue of International Journal of Environmental Research and Public Health (ISSN 1660-4601). This special issue belongs to the section "Environmental Ecology".

Deadline for manuscript submissions: closed (31 August 2023) | Viewed by 17398

Special Issue Editors


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Guest Editor
Department of Hydrobiology and Protection of Ecosystems, University of Life Sciences in Lublin, 20-262 Lublin, Poland
Interests: cyanobacterial blooms and toxicity; ecology of phytoplankton and phytobenthos of freshwaters
Special Issues, Collections and Topics in MDPI journals

E-Mail Website
Guest Editor
Department of Hydrobiology and Protection of Ecosystems, University of Life Sciences in Lublin, 20-262 Lublin, Poland
Interests: hydrology; lake-catchment processes; limnology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

In recent decades, climate changes and progressive water eutrophication have contributed to the intensification of cyanobacterial blooms worldwide. Blooms and the production of cyanobacterial toxins and other biologically active metabolites (such as oligopeptide anabaenopeptins, aeruginosins, cyanopeptolins etc.) may strongly affect various aquatic organisms and ecosystems, as well as pose a risk to human health. Due to limited and decreasing freshwater resources, studies on the causes and consequences of harmful cyanobacterial blooms (HCBs) are a burning need. For example, research on climatic conditions and hydro-chemical processes responsible for cyanobacterial massive development is of extreme importance. Also, the fate of cyanobacterial metabolites and their impact on aquatic organisms and ecosystems are extremely important, especially in light of the discoveries of new biologically active cyanobacterial compounds.

In particular, this Special Issue welcomes papers on:

  • environmental (climatic, hydrological etc.) conditions for the formation of cyanobacterial blooms in fresh-, brackish-, and marine waters;
  • monitoring of toxic cyanobacterial blooms, metabolites, and metabolites’ transformation products in aquatic environments;
  • factors influencing the bioaccumulation, biotransformation, and decomposition of cyanobacterial metabolites;
  • structural characterization of new cyanobacterial metabolites;
  • biology, ecology, and monitoring of aquatic organisms living in ecosystems affected by cyanobacterial blooms;
  • the influence of cyanotoxins and other cyanobacterial metabolites on aquatic organisms, ecosystems and human health: risk assessment;
  • the development of monitoring systems of cyanobacterial metabolites in waters and assessment of aquatic toxicity: scaling techniques, dynamic models, biological indicators;
  • role of modeling and remote sensing measurements as tools in HCBs management.

Both original research papers and review papers are welcomed.

Dr. Magdalena Toporowska
Dr. Beata Ferencz
Guest Editors

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Keywords

  • cyanotoxins
  • microcystins
  • anatoxins
  • oligopeptides
  • toxicity tests
  • biotransformation
  • climate changes
  • hydrological regime
  • monitoring
  • remote sensing

Published Papers (10 papers)

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Research

17 pages, 4576 KiB  
Article
Ecological Implications in a Human-Impacted Lake—A Case Study of Cyanobacterial Blooms in a Recreationally Used Water Body
by Agnieszka Napiórkowska-Krzebietke, Julita Anna Dunalska and Elżbieta Bogacka-Kapusta
Int. J. Environ. Res. Public Health 2023, 20(6), 5063; https://doi.org/10.3390/ijerph20065063 - 13 Mar 2023
Cited by 1 | Viewed by 1346
Abstract
This study was aimed primarily at describing the planktonic assemblages with special attention to invasive and toxin-producing cyanobacterial species in the context of ecological and health threats. The second aim was to analyze the aspect of recreational pressure, which may enhance the cyanobacterial [...] Read more.
This study was aimed primarily at describing the planktonic assemblages with special attention to invasive and toxin-producing cyanobacterial species in the context of ecological and health threats. The second aim was to analyze the aspect of recreational pressure, which may enhance the cyanobacterial blooms, and, as a consequence, the negative changes and loss of planktonic biodiversity. This study was carried out in recreationally used Lake Sztynorckie throughout the whole growing season of 2020 and included an assessment of the abundance and biomass of phytoplankton (cyanobacteria and algae) in relation to environmental variables. The total biomass was in the range of 28–70 mg L−1, which is typical for strong blooms. The dominant filamentous cyanobacteria were Pseudanabaena limnetica, Limnothrix redekei, Planktolyngbya limnetica, and Planktothrix agarhii, and three invasive nostocalean species Sphaerospermopsis aphanizomenoides, Cuspidothrix issatschenkoi, and Raphidiopsis raciborskii. They can pose a serious threat not only to the ecosystem but also to humans because of the possibility of cyanobacteria producing cyanotoxins, such as microcystins, saxitoxins, anatoxin-a, and cylindrospermopsins, having hepatotoxic, cytotoxic, neurotoxic, and dermatoxic effects. The water quality was assessed as water bodies had bad ecological status (based on phytoplankton), were highly meso-eutrophic (based on zooplankton), and had very low trophic efficiency and low biodiversity. Full article
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12 pages, 591 KiB  
Article
Non-Nitrogen-Fixers or Nitrogen-Fixers? Factors Distinguishing the Dominance of Chroococcal and Diazotrophic Cyanobacterial Species
by Elżbieta Wilk-Woźniak, Ewa Szarek-Gwiazda, Edward Walusiak, Joanna Kosiba and Wojciech Krztoń
Int. J. Environ. Res. Public Health 2022, 19(23), 15980; https://doi.org/10.3390/ijerph192315980 - 30 Nov 2022
Viewed by 1033
Abstract
Global warming and eutrophication are the main factors driving the development of cyanobacterial dominance in aquatic ecosystems. We used a model linking water temperature, oxygen saturation, concentrations of PO43−, NO3, NH4+, total dissolved iron [...] Read more.
Global warming and eutrophication are the main factors driving the development of cyanobacterial dominance in aquatic ecosystems. We used a model linking water temperature, oxygen saturation, concentrations of PO43−, NO3, NH4+, total dissolved iron (TDFe), and SO42− to cyanobacteria to test the turnover patterns of cyanobacterial dominance of non-nitrogen-fixing (chroococcal species) and nitrogen-fixing (filamentous diazotrophic) species. Statistical analysis was performed using decision trees. The dominance patterns of the two morphologically and ecologically distinct cyanobacterial species were associated with different environmental factors. However, SO42− was the most important factor that explained whether non-nitrogen-fixing or nitrogen-fixing species would dominate. Other important factors were water temperature, phosphate concentration, and oxygen saturation. The model for dominance of non-nitrogen-fixing species used SO42−, PO43−, and water temperature (upper layers), and SO42−, the ratio of PO43−/NH4+, and oxygen saturation (bottom layers). In contrast, water temperature, SO42−, and NH4+ in the upper layers and SO42−, NH4+, and water temperature in the bottom layers were used for the dominance of nitrogen-fixing species. The dominance of Aphanizomenon flos-aquae was explained by different sets of variables, indicating the presence of different strains of this species. The other cyanobacteria species showed dominance patterns that could be explained by one set of variables. As cyanobacterial blooms proliferate due to climate change, it is important to know which factors, in addition to phosphorus and nitrogen, are crucial for the mass development of the various cyanobacterial species. Full article
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15 pages, 2760 KiB  
Article
Cyanobacteria and Their Metabolites in Mono- and Polidominant Shallow Eutrophic Temperate Lakes
by Ksenija Savadova-Ratkus, Hanna Mazur-Marzec, Jūratė Karosienė, Kaarina Sivonen, Suvi Suurnäkki, Jūratė Kasperovičienė, Ričardas Paškauskas and Judita Koreivienė
Int. J. Environ. Res. Public Health 2022, 19(22), 15341; https://doi.org/10.3390/ijerph192215341 - 20 Nov 2022
Cited by 2 | Viewed by 1659
Abstract
Monodominant (one species dominates) or polidominant (multiple species dominate) cyanobacterial blooms are pronounced in productive freshwater ecosystems and pose a potential threat to the biota due to the synthesis of toxins. Seasonal changes in cyanobacteria species and cyanometabolites composition were studied in two [...] Read more.
Monodominant (one species dominates) or polidominant (multiple species dominate) cyanobacterial blooms are pronounced in productive freshwater ecosystems and pose a potential threat to the biota due to the synthesis of toxins. Seasonal changes in cyanobacteria species and cyanometabolites composition were studied in two shallow temperate eutrophic lakes. Data on cyanobacteria biomass and diversity of dominant species in the lakes were combined with chemical and molecular analyses of fifteen potentially toxin-producing cyanobacteria species (248 isolates from the lakes). Anatoxin-a, saxitoxin, microcystins and other non-ribosomal peptides formed the diverse profiles in monodominant (Planktothrix agardhii) and polidominant (Aphanizomenon gracile, Limnothrix spp. and Planktolyngbya limnetica) lakes. However, the harmfulness of the blooms depended on the ability of the dominant species to synthesize cyanometabolites. It was confirmed that P. agardhii produced a greater amount and diverse range of MCs and other NRPs. In the polidominant lake, isolates of the co-dominant A. gracile, L. planctonica and P. limnetica synthesized no or only small amounts of cyanometabolites. In general, the profile of cyanometabolites was greater in cyanobacteria isolates than in environmental samples, indicating a high potential for toxic cyanobacteria bloom. Full article
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11 pages, 495 KiB  
Article
Interactions between Ciliate Species and Aphanizomenon flos-aquae Vary Depending on the Morphological Form and Biomass of the Diazotrophic Cyanobacterium
by Joanna Kosiba, Wojciech Krztoń, Judita Koreiviené, Sebastian Tarcz and Elżbieta Wilk-Woźniak
Int. J. Environ. Res. Public Health 2022, 19(22), 15097; https://doi.org/10.3390/ijerph192215097 - 16 Nov 2022
Cited by 2 | Viewed by 1445
Abstract
Aphanizomenon flos-aquae can form extensive blooms from freshwater to the brackish environment and, being a diazotrophic species, contribute significantly to the nitrogen and carbon cycle. It occurs as single filaments or aggregates and could be used as an alternative nutrients source for bacteria and [...] Read more.
Aphanizomenon flos-aquae can form extensive blooms from freshwater to the brackish environment and, being a diazotrophic species, contribute significantly to the nitrogen and carbon cycle. It occurs as single filaments or aggregates and could be used as an alternative nutrients source for bacteria and ciliates. Ciliates are a group of organisms playing a crucial role in the transfer of nitrogen from primary producers to higher trophic levels in aquatic food webs. The aim of the experiment was to study the effects of the cyanobacterium A. flos-aquae on the community of five ciliate species (Spirostomum minus, Euplotes aediculatus, Strobilidium sp., Vorticella sp. and Paramecium tetraurelia). The response of each species to the presence of a low/high cyanobacterial biomass and to the different morphological forms of A. flos-aquae (single filaments or aggregates) was demonstrated. The results of the experiment showed the variability of interactions between the cyanobacterium A. flos-aquae and ciliates and pointed out the possible benefits that A. flos-aquae provides to the ciliates (e.g., a substrate for the development of bacteria as food for ciliates or as a source of nitrogen and carbon). Full article
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18 pages, 2867 KiB  
Article
Planktothrix agardhii versus Planktothrix rubescens: Separation of Ecological Niches and Consequences of Cyanobacterial Dominance in Freshwater
by Tomasz Lenard and Małgorzata Poniewozik
Int. J. Environ. Res. Public Health 2022, 19(22), 14897; https://doi.org/10.3390/ijerph192214897 - 12 Nov 2022
Cited by 3 | Viewed by 1524
Abstract
Cyanobacteria dominate lakes under diverse trophic conditions. Of these, two harmful filamentous cyanobacterial species, namely Planktothrix agardhii and P. rubescens, occupy completely different ecological niches in which they can form dense populations. In the present study, we investigated the effects of environmental [...] Read more.
Cyanobacteria dominate lakes under diverse trophic conditions. Of these, two harmful filamentous cyanobacterial species, namely Planktothrix agardhii and P. rubescens, occupy completely different ecological niches in which they can form dense populations. In the present study, we investigated the effects of environmental conditions on the growth and vertical distribution of these species in lakes of different trophic statuses. Moreover, we underscored certain inconveniences in the assessment of the ecological status of lakes according to the European Union Water Framework Directive. The highest biomass of P. agardhii was recorded in eutrophic lake at a depth of 0.5–1 m, under high light intensity. Meanwhile, the highest biomass of P. rubescens, at which the deep chlorophyll maximum was recorded, was observed in mesotrophic lakes at a depth of 11–12 m, often below the euphotic zone under very low light intensity. P. rubescens, but not P. agardhii, exerted a strong allelopathic effect on the diversity and biomass of phytoplankton. Moreover, both species utilised different dissolved nitrogen fractions for their growth; specifically, P. agardhii used ammonium nitrogen, whilst P. rubescens used nitrate nitrogen. Furthermore, dissolved phosphorus produced a potentially limiting effect on P. rubescens growth. Overall, the tested Polish PMPL, German PSI, and Estonian phytoplankton indices were indeed useful in the assessment of the ecological status of lakes, albeit limited to the eutrophic lake with a high biomass of cyanobacteria (P. agardhii) in the upper water layers. However, problems arose in the proper assessment of lakes with a high biomass of cyanobacteria (P. rubescens) with a deep chlorophyll maximum outside the range of the euphotic zone. In such cases, two of the tested indices, namely the Polish and German indices, allowed sample collection from the euphotic layers, which significantly affected the number of samples included in the calculation. Consequently, the correct calculation of the ecological status of the lake was uncertain. Only the Estonian index allowed for a sample collection from two to three thermal layers of water, including the bloom layer of P. rubescens. Hence, the Estonian index offered the best fit for calculations. Full article
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15 pages, 6080 KiB  
Article
Anabaenopeptins from Nostoc edaphicum CCNP1411
by Robert Konkel, Michał Grabski, Marta Cegłowska, Ewa Wieczerzak, Grzegorz Węgrzyn and Hanna Mazur-Marzec
Int. J. Environ. Res. Public Health 2022, 19(19), 12346; https://doi.org/10.3390/ijerph191912346 - 28 Sep 2022
Cited by 2 | Viewed by 1860
Abstract
Cyanobacteria of the Nostoc genus belong to the most prolific sources of bioactive metabolites. In our previous study on Nostoc edaphicum strain CCNP1411, the occurrence of cyanopeptolins and nostocyclopeptides was documented. In the current work, the production of anabaenopeptins (APs) by the strain [...] Read more.
Cyanobacteria of the Nostoc genus belong to the most prolific sources of bioactive metabolites. In our previous study on Nostoc edaphicum strain CCNP1411, the occurrence of cyanopeptolins and nostocyclopeptides was documented. In the current work, the production of anabaenopeptins (APs) by the strain was studied using genetic and chemical methods. Compatibility between the analysis of the apt gene cluster and the structure of the identified APs was found. Three of the APs, including two new variants, were isolated as pure compounds and tested against four serine proteases and carboxypeptidase A (CPA). The in vitro enzymatic assays showed a typical activity of this class of cyanopeptides, i.e., the most pronounced effects were observed in the case of CPA. The activity of the detected compounds against important metabolic enzymes confirms the pharmaceutical potential of anabaenopeptins. Full article
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17 pages, 5904 KiB  
Article
Persistent Cyanobacteria Blooms in Artificial Water Bodies—An Effect of Environmental Conditions or the Result of Anthropogenic Change
by Paulina Nowicka-Krawczyk, Joanna Żelazna-Wieczorek, Izabela Skrobek, Maciej Ziułkiewicz, Michał Adamski, Ariel Kaminski and Paweł Żmudzki
Int. J. Environ. Res. Public Health 2022, 19(12), 6990; https://doi.org/10.3390/ijerph19126990 - 7 Jun 2022
Cited by 8 | Viewed by 2263
Abstract
Algal blooms are an emerging problem. The massive development of phytoplankton is driven partly by the anthropogenic eutrophication of aquatic ecosystems and the expansion of toxic cyanobacteria in planktonic communities in temperate climate zones by the continual increase in global temperature. Cyanobacterial harmful [...] Read more.
Algal blooms are an emerging problem. The massive development of phytoplankton is driven partly by the anthropogenic eutrophication of aquatic ecosystems and the expansion of toxic cyanobacteria in planktonic communities in temperate climate zones by the continual increase in global temperature. Cyanobacterial harmful algal blooms (CyanoHABs) not only disturb the ecological balance of the ecosystem, but they also prevent the use of waterbodies by humans. This study examines the cause of an unusual, persistent bloom in a recreational, flow-through reservoir; the findings emphasize the role played by the river supplying the reservoir in the formation of its massive cyanobacterial bloom. Comprehensive ecosystem-based environmental studies were performed, including climate change investigation, hydrochemical analysis, and bio-assessment of the ecological state of the river/reservoir, together with monitoring the cyanobacteria content of phytoplankton. Our findings show that the persistent and dominant biomass of Microcystis was related to the N/P ratio, while the presence of Aphanizomenon and Dolichospermum was associated with the high-temperature end electric conductivity of water. Together with the increase in global temperature, the massive and persistent cyanobacterial bloom appears to be maintained by the inflow of biogenic compounds carried by the river and the high electric conductivity of water. Even at the beginning of the phenomenon, the reservoir water already contained cyanobacterial toxins, which excluded its recreational use for about half the year. Full article
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17 pages, 2733 KiB  
Article
Degradation of Three Microcystin Variants in the Presence of the Macrophyte Spirodela polyrhiza and the Associated Microbial Communities
by Magdalena Toporowska
Int. J. Environ. Res. Public Health 2022, 19(10), 6086; https://doi.org/10.3390/ijerph19106086 - 17 May 2022
Cited by 4 | Viewed by 1598
Abstract
Cyanobacteria, which form water blooms all over the world, can produce a wide range of cyanotoxins such as hepatotoxic microcystins (MCs) and other biologically active metabolites harmful to living organisms, including humans. Microcystin biodegradation, particularly caused by bacteria, has been broadly documented; however, [...] Read more.
Cyanobacteria, which form water blooms all over the world, can produce a wide range of cyanotoxins such as hepatotoxic microcystins (MCs) and other biologically active metabolites harmful to living organisms, including humans. Microcystin biodegradation, particularly caused by bacteria, has been broadly documented; however, studies in this field focus mainly on strains isolated from natural aquatic environments. In this paper, the biodegradation of microcystin-RR (MC-RR), microcystin-LR (MC-LR), and microcystin-LF (MC-LF) after incubation with Spirodela polyrhiza and the associated microorganisms (which were cultured under laboratory conditions) is shown. The strongest MC biodegradation rate after nine days of incubation was observed for MC-RR, followed by MC-LR. No statistically significant decrease in the concentration of MC-LF was noted. Products of MC decomposition were detected via the HPLC method, and their highest number was found for MC-RR (six products with the retention time between 5.6 and 16.2 min), followed by MC-LR (two products with the retention time between 19.3 and 20.2 min). Although the decrease in MC-LF concentration was not significant, four MC-LF degradation products were detected with the retention time between 28.9 and 33.0 min. The results showed that MC-LF was the most stable and resistant MC variant under experimental conditions. No accumulation of MCs or their biodegradation products in S. polyrhiza was found. The findings suggest that the microorganisms (bacteria and algae) associated with S. polyrhiza could be responsible for the MC biodegradation observed. Therefore, there is a need to broaden the research on the biodegradation products detected and potential MC-degraders associated with plants. Full article
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13 pages, 2008 KiB  
Article
Phytoplankton Sensitivity to Heavy Metals in Baltic Coastal Lakes
by Monika Szymańska-Walkiewicz, Katarzyna Glińska-Lewczuk, Paweł Burandt and Krystian Obolewski
Int. J. Environ. Res. Public Health 2022, 19(7), 4131; https://doi.org/10.3390/ijerph19074131 - 31 Mar 2022
Cited by 10 | Viewed by 1749
Abstract
This study aimed to compare concentrations of chlorophyll-a between individual phytoplankton groups for four shallow Baltic coastal lakes, varying in type of connection with the sea. For two years, the research focused on quantifying the effects of abiotic factors—concentrations of heavy metals (Ba, [...] Read more.
This study aimed to compare concentrations of chlorophyll-a between individual phytoplankton groups for four shallow Baltic coastal lakes, varying in type of connection with the sea. For two years, the research focused on quantifying the effects of abiotic factors—concentrations of heavy metals (Ba, Bi, Cr, Cu, Mn, Fe, Ni, Pb, and Zn) and hydrological connectivity—on phytoplankton composition, biomass, and photosynthetic activity. Our results show that hydrological factors are the main predictors of phytoplankton structure. The lakes differed in salinity: freshwater vs. brackish vs. transitional lakes. Irrespective of lake type, the dominant group was that of Cyanobacteria (~80%), but their percentage contribution was lower in the brackish lake. Baltic seawater intrusion resulted in a decrease in heavy-metal concentrations in lake water for Fe, Zn, Pb, and Bi. Redundancy analysis (RDA) suggested positive effects of some heavy metals on the biomass of the Chlorophyta and Bacillariophyta. For the Cryptophyta only, a slight decrease in biomass was linked with increased metal concentrations in open water. Full article
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17 pages, 1398 KiB  
Article
Phytoplankton Composition and Ecological Status of Lakes with Cyanobacteria Dominance
by Małgorzata Poniewozik and Tomasz Lenard
Int. J. Environ. Res. Public Health 2022, 19(7), 3832; https://doi.org/10.3390/ijerph19073832 - 23 Mar 2022
Cited by 6 | Viewed by 1911
Abstract
Phytoplankton is one of the five biological quality elements used in the assessment of the ecological status of surface waters according to the European Water Framework Directive established in 2000. In this study, we determined the ecological status of three small and shallow [...] Read more.
Phytoplankton is one of the five biological quality elements used in the assessment of the ecological status of surface waters according to the European Water Framework Directive established in 2000. In this study, we determined the ecological status of three small and shallow lakes in the Polesie Plain, Eastern Poland, by using indices based on phytoplankton assemblages. The predominant phytoplankton of all three lakes were filamentous cyanobacteria, both heterocystous and non-heterocystous, represented by the genera Aphanizomenon, Planktothrix, Limnothrix, and Planktolyngbya. We used the Hungarian Q index, German PSI (Phyto-See-Index), and recently developed PMPL (Phytoplankton Metrics for Polish Lakes) for Polish lakes. We compared the results from the calculation of the indices to physicochemical data obtained from the lake water and Carlson’s Trophy State Index (TSI). On the basis of TSI, Gumienek and Glinki lakes were classified as advanced eutrophic, whereas Czarne Lake had a better score and was classified as slightly eutrophic. The trophic state was generally confirmed by the ecological status based on phytoplankton indices and also showed the diverse ecological situation in the lakes studied. Based on the Polish PMPL, Gumienek Lake was classified as having bad status (ecological quality ratio (EQR) = 0.05), whereas Glinki and Czarne lakes were classified within the poor status range (EQR = 0.25 and 0.35, respectively). However, based on the German PSI, the lakes were classified in a different manner: the status of Gumienek and Czarne lakes was better, but unsatisfactory, because they were still below the boundary for the good status category recommended by the European Commission. The best ecological status for the studied lakes was obtained using the Q index: Gumienek Lake with EQR = 0.42 had a moderate status, and Czarne Lake with EQR = 0.62 obtained a good status. However, Glinki Lake, with EQR = 0.40, was classified at the boundary for poor and moderate status. Based on our study, it seems that the best index for ecological status assessment based on phytoplankton that can be used for small lakes is the Polish (PMPL) index. Full article
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