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Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics

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A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Marine and Freshwater Toxins".

Deadline for manuscript submissions: closed (31 January 2020) | Viewed by 41153

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Dr. Petra M. Visser

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Guest Editor

Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Sciencepark 904, P.O. Box 94240, 1090 GE Amsterdam, The Netherlands
Interests: cyanobacteria; cyanotoxins; microcystins; control and mitigation of cyanobacterial blooms; hydrogen peroxide; artificial mixing; physiology; ecology; benthic cyanobacterial mats; coral reefs; marine cyanobacteria

Dr. Dedmer B. Van de Waal

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Guest Editor

Department of Aquatic Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands

Special Issue Information

Dear Colleagues,

Harmful algal and cyanobacterial blooms pose an eminent threat to human and ecosystem health. Toxicity of blooms depends on a range of factors across multiple scales from community down to the cellular level. Specifically, it depends on the total biomass of toxic species, the identity of these species and associated toxin compounds, the abundance of toxic genotypes, the cellular quantities of toxins in these genotypes, and the toxin analogue composition. Environmental factors, both abiotic and biotic, are known to alter different aspects of bloom toxin contents. For instance, studies in marine and freshwater harmful algal or cyanobacterial species have reported effects of resource concentrations (nutrients, light, inorganic carbon, iron, etc.) and trophic interactions (e.g. zooplankton exudates, allelopathic compounds) on biomass build-up, genotype composition, cellular toxin content, expression of toxin genes, and toxin composition of the bloom. Here, we aim at collecting recent studies that cover any of the above aspects determining bloom toxicity across taxonomic groups and ecosystems to provide an integrated view on key environmental drivers underlying toxin dynamics in harmful algal and cyanobacterial blooms.

Dr. Petra M. Visser
Dr. Dedmer B. van de Waal
Guest Editors

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Keywords

HABs
eutrophication
phycotoxins
cyanotoxins
blooms
phytoplankton
benthic
marine
freshwater
toxin production

Published Papers (10 papers)

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Research

13 pages, 1606 KiB

Open AccessEditor’s ChoiceArticle

Effects of Nutrient Limitation on the Synthesis of N-Rich Phytoplankton Toxins: A Meta-Analysis

by Karen Brandenburg, Laura Siebers, Joost Keuskamp, Thomas G. Jephcott and Dedmer B. Van de Waal

Toxins 2020, 12(4), 221; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12040221 - 01 Apr 2020

Cited by 36 | Viewed by 4471

Abstract

Eutrophication has played a major role in the worldwide increase of harmful algal blooms (HABs). Higher input of key nutrients, such as nitrogen (N) and phosphorus (P), can stimulate the growth of harmful algal species in freshwater, estuarine, and coastal marine ecosystems. Some HAB-forming taxa, particularly several cyanobacteria and dinoflagellate species, are harmful through the production of N-rich toxins that have detrimental effects on the environment and human health. Here, we test how changes in nutrient availability affect N-rich toxin synthesis in cyanobacteria and dinoflagellates using a meta-analysis approach. Overall, N-rich toxin content showed an increase with P limitation, while it tended to decrease with N limitation, but we also observed substantial variation in responses both within and across genera and toxin groups. For instance, in response to N limitation, microcystin content varied from a 297% decrease up to a 273% increase, and paralytic shellfish poisoning (PSP) toxin content varied from a 204% decrease to an 82% increase. Cylindrospermopsin, produced by N₂-fixing cyanobacteria, showed no clear direction in response to nutrient limitation, and cellular contents of this compound may thus vary independently of nutrient fluctuations. Our results confirm earlier reported stoichiometric regulation of N-rich phytoplankton toxins, showing increased toxin content with an increase in cellular N:P ratios, and vice versa. Thus, changes in N-rich toxin content largely follow the changes in relative cellular N content. Consequently, although nutrient limitation may limit bloom biomass and thereby bloom toxicity, our results warn that P limitation can cause accumulation of cellular toxins and thus lead to unexpected increases in bloom toxicity. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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21 pages, 3624 KiB

Open AccessArticle

Using Microcystin Gene Copies to Determine Potentially-Toxic Blooms, Example from a Shallow Eutrophic Lake Peipsi

by Kristel Panksep, Marju Tamm, Evanthia Mantzouki, Anne Rantala-Ylinen, Reet Laugaste, Kaarina Sivonen, Olga Tammeorg and Veljo Kisand

Toxins 2020, 12(4), 211; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12040211 - 26 Mar 2020

Cited by 7 | Viewed by 3821

Abstract

Global warming, paired with eutrophication processes, is shifting phytoplankton communities towards the dominance of bloom-forming and potentially toxic cyanobacteria. The ecosystems of shallow lakes are especially vulnerable to these changes. Traditional monitoring via microscopy is not able to quantify the dynamics of toxin-producing cyanobacteria on a proper spatio-temporal scale. Molecular tools are highly sensitive and can be useful as an early warning tool for lake managers. We quantified the potential microcystin (MC) producers in Lake Peipsi using microscopy and quantitative polymerase chain reaction (qPCR) and analysed the relationship between the abundance of the mcyE genes, MC concentration, MC variants and toxin quota per mcyE gene. We also linked environmental factors to the cyanobacteria community composition. In Lake Peipsi, we found rather moderate MC concentrations, but microcystins and microcystin-producing cyanobacteria were widespread across the lake. Nitrate (NO₃⁻) was a main driver behind the cyanobacterial community at the beginning of the growing season, while in late summer it was primarily associated with the soluble reactive phosphorus (SRP) concentration. A positive relationship was found between the MC quota per mcyE gene and water temperature. The most abundant variant—MC-RR—was associated with MC quota per mcyE gene, while other MC variants did not show any significant impact. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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18 pages, 3268 KiB

Open AccessArticle

Salt Shock Responses of Microcystis Revealed through Physiological, Transcript, and Metabolomic Analyses

by Maxime Georges des Aulnois, Damien Réveillon, Elise Robert, Amandine Caruana, Enora Briand, Arthur Guljamow, Elke Dittmann, Zouher Amzil and Myriam Bormans

Toxins 2020, 12(3), 192; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12030192 - 18 Mar 2020

Cited by 14 | Viewed by 3661

Abstract

The transfer of Microcystis aeruginosa from freshwater to estuaries has been described worldwide and salinity is reported as the main factor controlling the expansion of M. aeruginosa to coastal environments. Analyzing the expression levels of targeted genes and employing both targeted and non-targeted metabolomic approaches, this study investigated the effect of a sudden salt increase on the physiological and metabolic responses of two toxic M. aeruginosa strains separately isolated from fresh and brackish waters, respectively, PCC 7820 and 7806. Supported by differences in gene expressions and metabolic profiles, salt tolerance was found to be strain specific. An increase in salinity decreased the growth of M. aeruginosa with a lesser impact on the brackish strain. The production of intracellular microcystin variants in response to salt stress correlated well to the growth rate for both strains. Furthermore, the release of microcystins into the surrounding medium only occurred at the highest salinity treatment when cell lysis occurred. This study suggests that the physiological responses of M. aeruginosa involve the accumulation of common metabolites but that the intraspecific salt tolerance is based on the accumulation of specific metabolites. While one of these was determined to be sucrose, many others remain to be identified. Taken together, these results provide evidence that M. aeruginosa is relatively salt tolerant in the mesohaline zone and microcystin (MC) release only occurs when the capacity of the cells to deal with salt increase is exceeded. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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20 pages, 2382 KiB

Open AccessArticle

Phosphate Limitation Increases Content of Protease Inhibitors in the Cyanobacterium Microcystis aeruginosa

by Christian Burberg, Thomas Petzoldt and Eric von Elert

Toxins 2020, 12(1), 33; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12010033 - 06 Jan 2020

Cited by 9 | Viewed by 3365

Abstract

Increased anthropogenic nutrient input has led to eutrophication of lakes and ponds, resulting worldwide in more frequent and severe cyanobacterial blooms. In particular, enhanced availability of phosphorus (P) can promote cyanobacterial mass developments and may affect the content of secondary metabolites in cyanobacteria, such as protease inhibitors (PIs). PIs are common among cyanobacteria and have been shown to negatively affect herbivorous zooplankton. Here, we test the hypothesis that P-limitation reduces the growth of Microcystis, but increases the content of PIs. In batch culture experiments with eight different initial phosphate concentrations (5–75 µM) we determined growth, stoichiometry, and PI content of Microcystis aeruginosa NIVA Cya 43. This strain produces the protease inhibitor BN920 that is converted by chlorination to CP954, which constitutes the major PI in this strain. C:N:P-ratios of the biomass indicated variation of P-limitation with treatment and time. When normalized to biomass, the PI content varied up to nearly nineteen-fold with treatment and time and was highest in the low-P treatments, especially during the mid-exponential growth phase. However, these effects were alleviated under nitrogen co-limitation. The content of CP954 showed an inverse u-shaped response to growth rate and C:N-ratio of the cyanobacterial biomass, whereas it increased with cyanobacterial C:P. The results indicate that P-limitation supports a higher content of defensive PIs and may indirectly foster cyanobacterial blooms by increasing the negative interference of cyanobacteria with their consumers. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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16 pages, 1322 KiB

Open AccessArticle

High Diversity of Microcystin Chemotypes within a Summer Bloom of the Cyanobacterium Microcystis botrys

by Emma Johansson, Catherine Legrand, Caroline Björnerås, Anna Godhe, Hanna Mazur-Marzec, Torbjörn Säll and Karin Rengefors

Toxins 2019, 11(12), 698; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11120698 - 01 Dec 2019

Cited by 6 | Viewed by 3508

Abstract

The fresh-water cyanobacterium Microcystis is known to form blooms world-wide, and is often responsible for the production of microcystins found in lake water. Microcystins are non-ribosomal peptides with toxic effects, e.g. on vertebrates, but their function remains largely unresolved. Moreover, not all strains produce microcystins, and many different microcystin variants have been described. Here we explored the diversity of microcystin variants within Microcystis botrys, a common bloom-former in Sweden. We isolated a total of 130 strains through the duration of a bloom in eutrophic Lake Vomb, and analyzed their microcystin profiles with tandem mass spectrometry (LC-MS/MS). We found that microcystin producing (28.5%) and non-producing (71.5%) M. botrys strains, co-existed throughout the bloom. However, microcystin producing strains were more prevalent towards the end of the sampling period. Overall, 26 unique M. botrys chemotypes were identified, and while some chemotypes re-occurred, others were found only once. The M. botrys chemotypes showed considerable variation both in terms of number of microcystin variants, as well as in what combinations the variants occurred. To our knowledge, this is the first report on microcystin chemotype variation and dynamics in M. botrys. In addition, our study verifies the co-existence of microcystin and non-microcystin producing strains, and we propose that environmental conditions may be implicated in determining their composition. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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17 pages, 3016 KiB

Open AccessEditor’s ChoiceArticle

Biological Stoichiometry Regulates Toxin Production in Microcystis aeruginosa (UTEX 2385)

by Nicole D. Wagner, Felicia S. Osburn, Jingyu Wang, Raegyn B. Taylor, Ashlynn R. Boedecker, C. Kevin Chambliss, Bryan W. Brooks and J. Thad Scott

Toxins 2019, 11(10), 601; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11100601 - 16 Oct 2019

Cited by 40 | Viewed by 4779

Abstract

Harmful algal blooms (HABs) are increasing in magnitude, frequency, and duration globally. Even though a limited number of phytoplankton species can be toxic, they are becoming one of the greatest water quality threats to public health and ecosystems due to their intrinsic toxicity to humans and the numerous interacting factors that undermine HAB forecasting. Here, we show that the carbon:nitrogen:phosphorus (C:N:P) stoichiometry of a common toxic phytoplankton species, Microcystis, regulates toxin quotas during blooms through a tradeoff between primary and secondary metabolism. Populations with optimal C:N (< 8) and C:P (< 200) cellular stoichiometry consistently produced more toxins than populations exhibiting stoichiometric plasticity. Phosphorus availability in water exerted a strong control on population biomass and C:P stoichiometry, but N availability exerted a stronger control on toxin quotas by regulating population biomass and C:N:P stoichiometry. Microcystin-LR, like many phytoplankton toxins, is an N-rich secondary metabolite with a C:N stoichiometry that is similar to the optimal growth stoichiometry of Microcystis. Thus, N availability relative to P and light provides a dual regulatory mechanism that controls both biomass production and cellular toxin synthesis. Overall, our results provide a quantitative framework for improving forecasting of toxin production during HABs and compelling support for water quality management that limit both N and P inputs from anthropogenic sources. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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22 pages, 3488 KiB

Open AccessEditor’s ChoiceArticle

A Multiplex Analysis of Potentially Toxic Cyanobacteria in Lake Winnipeg during the 2013 Bloom Season

by Katelyn M. McKindles, Paul V. Zimba, Alexander S. Chiu, Susan B. Watson, Danielle B. Gutierrez, Judy Westrick, Hedy Kling and Timothy W. Davis

Toxins 2019, 11(10), 587; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11100587 - 11 Oct 2019

Cited by 15 | Viewed by 3858

Abstract

Lake Winnipeg (Manitoba, Canada), the world’s 12th largest lake by area, is host to yearly cyanobacterial harmful algal blooms (cHABs) dominated by Aphanizomenon and Dolichospermum. cHABs in Lake Winnipeg are primarily a result of eutrophication but may be exacerbated by the recent introduction of dreissenid mussels. Through multiple methods to monitor the potential for toxin production in Lake Winnipeg in conjunction with environmental measures, this study defined the baseline composition of a Lake Winnipeg cHAB to measure potential changes because of dreissenid colonization. Surface water samples were collected in 2013 from 23 sites during summer and from 18 sites in fall. Genetic data and mass spectrometry cyanotoxin profiles identified microcystins (MC) as the most abundant cyanotoxin across all stations, with MC concentrations highest in the north basin. In the fall, mcyA genes were sequenced to determine which species had the potential to produce MCs, and 12 of the 18 sites were a mix of both Planktothrix and Microcystis. Current blooms in Lake Winnipeg produce low levels of MCs, but the capacity to produce cyanotoxins is widespread across both basins. If dreissenid mussels continue to colonize Lake Winnipeg, a shift in physicochemical properties of the lake because of faster water column clearance rates may yield more toxic blooms potentially dominated by microcystin producers. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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20 pages, 2175 KiB

Open AccessEditor’s ChoiceArticle

Daphnia magna Exudates Impact Physiological and Metabolic Changes in Microcystis aeruginosa

by Gorenka Bojadzija Savic, Christine Edwards, Enora Briand, Linda Lawton, Claudia Wiegand and Myriam Bormans

Toxins 2019, 11(7), 421; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11070421 - 19 Jul 2019

Cited by 9 | Viewed by 4975

Abstract

While the intracellular function of many toxic and bioactive cyanobacterial metabolites is not yet known, microcystins have been suggested to have a protective role in the cyanobacterial metabolism, giving advantage to toxic over nontoxic strains under stress conditions. The zooplankton grazer Daphnia reduce cyanobacterial dominance until a certain density, which may be supported by Daphnia exudates, affecting the cyanobacterial physiological state and metabolites’ production. Therefore, we hypothesized that D. magna spent medium will impact the production of cyanobacterial bioactive metabolites and affect cyanobacterial photosynthetic activity in the nontoxic, but not the toxic strain. Microcystin (MC-LR and des-MC-LR) producing M. aeruginosa PCC7806 and its non-microcystin producing mutant were exposed to spent media of different D. magna densities and culture durations. D. magna spent medium of the highest density (200/L) cultivated for the shortest time (24 h) provoked the strongest effect. D.magna spent medium negatively impacted the photosynthetic activity of M. aeruginosa PCC7806, as well as the dynamics of intracellular and extracellular cyanobacterial metabolites, while its mutant was unaffected. In the presence of Daphnia medium, microcystin does not appear to have a protective role for the strain. On the contrary, extracellular cyanopeptolin A increased in M. aeruginosa PCC7806 although the potential anti-grazing role of this compound would require further studies. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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15 pages, 1272 KiB

Open AccessArticle

Development of an Indirect Quantitation Method to Assess Ichthyotoxic B-Type Prymnesins from Prymnesium parvum

by Daniel Killerup Svenssen, Sofie Bjørnholt Binzer, Nikola Medić, Per Juel Hansen, Thomas Ostenfeld Larsen and Elisabeth Varga

Toxins 2019, 11(5), 251; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11050251 - 04 May 2019

Cited by 7 | Viewed by 4059

Abstract

Harmful algal blooms of Prymnesium parvum have recurrently been associated with the killing of fish. The causative ichthyotoxic agents of this haptophyte are believed to be prymnesins, a group of supersized ladder-frame polyether compounds currently divided into three types. Here, the development of a quantitative method to assess the molar sum of prymnesins in water samples and in algal biomass is reported. The method is based on the derivatization of the primary amine group and subsequent fluorescence detection using external calibrants. The presence of prymnesins in the underivatized sample should be confirmed by liquid chromatography mass spectrometry. The method is currently only partly applicable to water samples due to the low amounts that are present. The growth and cellular toxin content of two B-type producing strains were monitored in batch cultures eventually limited by an elevated pH. The cellular toxin contents varied by a factor of ~2.5 throughout the growth cycle, with the highest amounts found in the exponential growth phase and the lowest in the stationary growth/death phases. The strain K-0081 contained ~5 times more toxin than K-0374. Further investigations showed that the majority of prymnesins were associated with the biomass (89% ± 7%). This study provides the basis for further investigations into the toxicity and production of prymnesins. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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16 pages, 3209 KiB

Open AccessArticle

Production of Cyanotoxins by Microcystis aeruginosa Mediates Interactions with the Mixotrophic Flagellate Cryptomonas

by Sarah DeVaul Princiotta, Susan P. Hendricks and David S. White

Toxins 2019, 11(4), 223; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11040223 - 15 Apr 2019

Cited by 17 | Viewed by 3796

Abstract

Eutrophication of inland waters is expected to increase the frequency and severity of harmful algal blooms (HABs). Toxin-production associated with HABs has negative effects on human health and aquatic ecosystem functioning. Despite evidence that flagellates can ingest toxin-producing cyanobacteria, interactions between members of the microbial loop are underestimated in our understanding of the food web and algal bloom dynamics. Physical and allelopathic interactions between a mixotrophic flagellate (Cryptomonas sp.) and two strains of a cyanobacteria (Microcystis aeruginosa) were investigated in a full-factorial experiment in culture. The maximum population growth rate of the mixotroph (0.25 day⁻¹) occurred during incubation with filtrate from toxic M. aeruginosa. Cryptomonas was able to ingest toxic and non-toxic M. aeruginosa at maximal rates of 0.5 and 0.3 cells day⁻¹, respectively. The results establish that although Cryptomonas does not derive benefits from co-incubation with M. aeruginosa, it may obtain nutritional supplement from filtrate. We also provide evidence of a reduction in cyanotoxin concentration (microcystin-LR) when toxic M. aeruginosa is incubated with the mixotroph. Our work has implications for “trophic upgrading” within the microbial food web, where cyanobacterivory by nanoflagellates may improve food quality for higher trophic levels and detoxify secondary compounds. Full article

(This article belongs to the Special Issue Environmental Drivers of Algal and Cyanobacterial Toxin Dynamics)

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