Biological Role of Cyanotoxins: Experimental and In-Field Evidence

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

Deadline for manuscript submissions: closed (15 April 2020) | Viewed by 24006

Special Issue Editor

Special Issue Information

Dear Colleagues,

Cyanobacteria are an ancient lineage of oxygenic photosynthetic bacteria found in a broad range of habitats, from soil to oceans, where they play important roles in the global nitrogen and carbon cycles. They are known for the toxic blooms they form in fresh water bodies around the world and the production of toxins, posing a threat to human and environmental health. Despite the tremendous effort to understand the biosynthesis, toxicity, and occurrence of cyanobacteria secondary metabolites, the biological role of these compounds still remains relatively unknown.  Various hypotheses in this regard have been put forward, encompassing both intracellular effects such as nutrient storage, light adaptation, and protection against oxidative stress, and extracellular functions including quorum sensing, allelopathic interactions, nutrient acquisition, colony formation, and grazing defense. The existing evidence on the potential role of cyanotoxins is mostly based on experimental studies and require further confirmation by in-field observations.

This Special Issue is destined to gather reviews, original experimental papers, and short notes reporting findings on experimental and in-field observations that aim to advance our understanding of the biological role of cyanotoxins. 

Dr. Piotr Rzymski
Guest Editors

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Keywords

  • Cyanobacteria
  • Cyanotoxins
  • Toxins
  • Allelopathy
  • Quorum sensing
  • Microcystins
  • Cylindrospermopsin
  • Anatoxin-a
  • Saxitoxins
  • Beta-methyl-amino-l-alanine
  • Nodularin.

Published Papers (5 papers)

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Research

Jump to: Review

24 pages, 2706 KiB  
Article
Proteomic Insights into Starvation of Nitrogen-Replete Cells of Nostoc sp. PCC 7120 under β-N-Methylamino-L-Alanine (BMAA) Treatment
by Olga A. Koksharova, Ivan O. Butenko, Olga V. Pobeguts, Nina A. Safronova and Vadim M. Govorun
Toxins 2020, 12(6), 372; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12060372 - 04 Jun 2020
Cited by 9 | Viewed by 3193
Abstract
All cyanobacteria produce a neurotoxic non-protein amino acid β-N-methylamino-L-alanine (BMAA). However, the biological function of BMAA in the regulation of cyanobacteria metabolism still remains undetermined. It is known that BMAA suppresses the formation of heterocysts in diazotrophic cyanobacteria under nitrogen starvation conditions, and [...] Read more.
All cyanobacteria produce a neurotoxic non-protein amino acid β-N-methylamino-L-alanine (BMAA). However, the biological function of BMAA in the regulation of cyanobacteria metabolism still remains undetermined. It is known that BMAA suppresses the formation of heterocysts in diazotrophic cyanobacteria under nitrogen starvation conditions, and BMAA induces the formation of heterocyst-like cells under nitrogen excess conditions, by causing the expression of heterocyst-specific genes that are usually “silent” under nitrogen-replete conditions, as if these bacteria receive a nitrogen deficiency intracellular molecular signal. In order to find out the molecular mechanisms underlying this unexpected BMAA effect, we studied the proteome of cyanobacterium Nostoc sp. PCC 7120 grown under BMAA treatment in nitrogen-replete medium. Experiments were performed in two experimental settings: (1) in control samples consisted of cells grown without the BMAA treatment and (2) the treated samples consisted of cells grown with addition of an aqueous solution of BMAA (20 µM). In total, 1567 different proteins of Nostoc sp. PCC 7120 were identified by LC-MS/MS spectrometry. Among them, 80 proteins belonging to different functional categories were chosen for further functional analysis and interpretation of obtained proteomic data. Here, we provide the evidence that a pleiotropic regulatory effect of BMAA on the proteome of cyanobacterium was largely different under conditions of nitrogen-excess compared to its effect under nitrogen starvation conditions (that was studied in our previous work). The most significant difference in proteome expression between the BMAA-treated and untreated samples under different growth conditions was detected in key regulatory protein PII (GlnB). BMAA downregulates protein PII in nitrogen-starved cells and upregulates this protein in nitrogen-replete conditions. PII protein is a key signal transduction protein and the change in its regulation leads to the change of many other regulatory proteins, including different transcriptional factors, enzymes and transporters. Complex changes in key metabolic and regulatory proteins (RbcL, RbcS, Rca, CmpA, GltS, NodM, thioredoxin 1, RpbD, ClpP, MinD, RecA, etc.), detected in this experimental study, could be a reason for the appearance of the “starvation” state in nitrogen-replete conditions in the presence of BMAA. In addition, 15 proteins identified in this study are encoded by genes, which are under the control of NtcA—a global transcriptional regulator—one of the main protein partners and transcriptional regulators of PII protein. Thereby, this proteomic study gives a possible explanation of cyanobacterium starvation under nitrogen-replete conditions and BMAA treatment. It allows to take a closer look at the regulation of cyanobacteria metabolism affected by this cyanotoxin. Full article
(This article belongs to the Special Issue Biological Role of Cyanotoxins: Experimental and In-Field Evidence)
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27 pages, 1728 KiB  
Article
The First Proteomic Study of Nostoc sp. PCC 7120 Exposed to Cyanotoxin BMAA under Nitrogen Starvation
by Olga A. Koksharova, Ivan O. Butenko, Olga V. Pobeguts, Nina A. Safronova and Vadim M. Govorun
Toxins 2020, 12(5), 310; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12050310 - 09 May 2020
Cited by 14 | Viewed by 4038
Abstract
The oldest prokaryotic photoautotrophic organisms, cyanobacteria, produce many different metabolites. Among them is the water-soluble neurotoxic non-protein amino acid beta-N-methylamino-L-alanine (BMAA), whose biological functions in cyanobacterial metabolism are of fundamental scientific and practical interest. An early BMAA inhibitory effect on nitrogen fixation and [...] Read more.
The oldest prokaryotic photoautotrophic organisms, cyanobacteria, produce many different metabolites. Among them is the water-soluble neurotoxic non-protein amino acid beta-N-methylamino-L-alanine (BMAA), whose biological functions in cyanobacterial metabolism are of fundamental scientific and practical interest. An early BMAA inhibitory effect on nitrogen fixation and heterocyst differentiation was shown in strains of diazotrophic cyanobacteria Nostoc sp. PCC 7120, Nostoc punctiforme PCC 73102 (ATCC 29133), and Nostoc sp. strain 8963 under conditions of nitrogen starvation. Herein, we present a comprehensive proteomic study of Nostoc (also called Anabaena) sp. PCC 7120 in the heterocyst formation stage affecting by BMAA treatment under nitrogen starvation conditions. BMAA disturbs proteins involved in nitrogen and carbon metabolic pathways, which are tightly co-regulated in cyanobacteria cells. The presented evidence shows that exogenous BMAA affects a key nitrogen regulatory protein, PII (GlnB), and some of its protein partners, as well as glutamyl-tRNA synthetase gltX and other proteins that are involved in protein synthesis, heterocyst differentiation, and nitrogen metabolism. By taking into account the important regulatory role of PII, it becomes clear that BMAA has a severe negative impact on the carbon and nitrogen metabolism of starving Nostoc sp. PCC 7120 cells. BMAA disturbs carbon fixation and the carbon dioxide concentrating mechanism, photosynthesis, and amino acid metabolism. Stress response proteins and DNA repair enzymes are upregulated in the presence of BMAA, clearly indicating severe intracellular stress. This is the first proteomic study of the effects of BMAA on diazotrophic starving cyanobacteria cells, allowing a deeper insight into the regulation of the intracellular metabolism of cyanobacteria by this non-protein amino acid. Full article
(This article belongs to the Special Issue Biological Role of Cyanotoxins: Experimental and In-Field Evidence)
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15 pages, 1906 KiB  
Article
Physiological Effects on Coexisting Microalgae of the Allelochemicals Produced by the Bloom-Forming Cyanobacteria Synechococcus sp. and Nodularia Spumigena
by Sylwia Śliwińska-Wilczewska, Aldo Barreiro Felpeto, Katarzyna Możdżeń, Vitor Vasconcelos and Adam Latała
Toxins 2019, 11(12), 712; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11120712 - 06 Dec 2019
Cited by 9 | Viewed by 2882
Abstract
Only a few studies have documented the physiological effects of allelopathy from cyanobacteria against coexisting microalgae. We investigated the allelopathic ability of the bloom-forming cyanobacteria Synechococcus sp. and Nodularia spumigena filtrates on several aspects related to the physiology of the target species: population [...] Read more.
Only a few studies have documented the physiological effects of allelopathy from cyanobacteria against coexisting microalgae. We investigated the allelopathic ability of the bloom-forming cyanobacteria Synechococcus sp. and Nodularia spumigena filtrates on several aspects related to the physiology of the target species: population growth, cell morphology, and several indexes of photosynthesis rate and respiration. The target species were the following: two species of green algae (Oocystis submarina, Chlorella vulgaris) and two species of diatoms (Bacillaria paxillifer, Skeletonema marinoi). These four species coexist in the natural environment with the employed strains of Synechococcus sp. and N. spumigena employed. The tests were performed with single and repeated addition of cyanobacterial cell-free filtrate. We also tested the importance of the growth phase in the strength of the allelopathic effect. The negative effects of both cyanobacteria were the strongest with repeated exudates addition, and generally, Synechococcus sp. and N. spumigena were allelopathic only in the exponential growth phase. O. submarina was not negatively affected by Synechococcus filtrates in any of the parameters studied, while C. vulgaris, B. paxillifer, and S. marinoi were affected in several ways. N. spumigena was characterized by a stronger allelopathic activity than Synechococcus sp., showing a negative effect on all target species. The highest decline in growth, as well as the most apparent cell physical damage, was observed for the diatom S. marinoi. Our findings suggest that cyanobacterial allelochemicals are associated with the cell physical damage, as well as a reduced performance in respiration and photosynthesis system in the studied microalgae which cause the inhibition of the population growth. Moreover, our study has shown that some biotic factors that increase the intensity of allelopathic effects may also alter the ratio between bloom-forming cyanobacteria and some phytoplankton species that occur in the same aquatic ecosystem. Full article
(This article belongs to the Special Issue Biological Role of Cyanotoxins: Experimental and In-Field Evidence)
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Review

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15 pages, 662 KiB  
Review
A Review on the Study of Cyanotoxins in Paleolimnological Research: Current Knowledge and Future Needs
by Eliana Henao, Piotr Rzymski and Matthew N. Waters
Toxins 2020, 12(1), 6; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins12010006 - 20 Dec 2019
Cited by 20 | Viewed by 4255
Abstract
Cyanobacterial metabolites are increasingly studied, in regards to their biosynthesis, ecological role, toxicity, and potential biomedical applications. However, the history of cyanotoxins prior to the last few decades is virtually unknown. Only a few paleolimnological studies have been undertaken to date, and these [...] Read more.
Cyanobacterial metabolites are increasingly studied, in regards to their biosynthesis, ecological role, toxicity, and potential biomedical applications. However, the history of cyanotoxins prior to the last few decades is virtually unknown. Only a few paleolimnological studies have been undertaken to date, and these have focused exclusively on microcystins and cylindrospermopsins, both successfully identified in lake sediments up to 200 and 4700 years old, respectively. In this paper, we review direct extraction, quantification, and application of cyanotoxins in sediment cores, and put forward future research prospects in this field. Cyanobacterial toxin research is also compared to other paleo-cyanobacteria tools, such as sedimentary pigments, akinetes, and ancient DNA isolation, to identify the role of each tool in reproducing the history of cyanobacteria. Such investigations may also be beneficial for further elucidation of the biological role of cyanotoxins, particularly if coupled with analyses of other abiotic and biotic sedimentary features. In addition, we identify current limitations as well as future directions for applications in the field of paleolimnological studies on cyanotoxins. Full article
(This article belongs to the Special Issue Biological Role of Cyanotoxins: Experimental and In-Field Evidence)
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19 pages, 790 KiB  
Review
Programmed Cell Death-Like and Accompanying Release of Microcystin in Freshwater Bloom-Forming Cyanobacterium Microcystis: From Identification to Ecological Relevance
by Chenlin Hu and Piotr Rzymski
Toxins 2019, 11(12), 706; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins11120706 - 04 Dec 2019
Cited by 44 | Viewed by 8809
Abstract
Microcystis is the most common freshwater bloom-forming cyanobacterium. Its massive blooms not only adversely affect the functionality of aquatic ecosystems, but are also associated with the production of microcystins (MCs), a group of potent toxins that become a threat to public health when [...] Read more.
Microcystis is the most common freshwater bloom-forming cyanobacterium. Its massive blooms not only adversely affect the functionality of aquatic ecosystems, but are also associated with the production of microcystins (MCs), a group of potent toxins that become a threat to public health when cell-bound MCs are significantly released from the dying Microcystis into the water column. Managing Microcystis blooms thus requires sufficient knowledge regarding both the cell death modes and the release of toxins. Recently, more and more studies have demonstrated the occurrence of programmed cell death-like (or apoptosis-like) events in laboratory and field samples of Microcystis. Apoptosis is a genetically controlled process that is essential for the development and survival of metazoa; however, it has been gradually realized to be an existing phenomenon playing important ecological roles in unicellular microorganisms. Here, we review the current progress and the existing knowledge gap regarding apoptosis-like death in Microcystis. Specifically, we focus first on the tools utilized to characterize the apoptosis-related biochemical and morphological features in Microcystis. We further outline various stressful stimuli that trigger the occurrence of apoptosis and discuss the potential mechanisms of apoptosis in Microcystis. We then propose a conceptual model to describe the functional coupling of apoptosis and MC in Microcystis. This model could be useful for understanding both roles of MC and apoptosis in this species. Lastly, we conclude the review by highlighting the current knowledge gap and considering the direction of future research. Overall, this review provides a recent update with respect to the knowledge of apoptosis in Microcystis and also offers a guide for future investigations of its ecology and survival strategies. Full article
(This article belongs to the Special Issue Biological Role of Cyanotoxins: Experimental and In-Field Evidence)
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