The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change

Climate change: links to global expansion of harmful cyanobacteria.

Cyanobacteria are the Earth's oldest known oxygen-evolving photosynthetic microorganisms, and they have had major impacts on shaping our current atmosphere and biosphere. Their long evolutionary history has enabled cyanobacteria to develop survival strategies and persist as important primary producers during numerous geochemical and climatic changes that have taken place on Earth during the past 3.5 billion years. Today, some cyanobacterial species form massive surface growths or 'blooms' that produce toxins, cause oxygen depletion and alter food webs, posing a major threat to drinking and irrigation water supplies, fishing and recreational use of surface waters worldwide. These harmful cyanobacteria can take advantage of anthropogenically induced nutrient over-enrichment (eutrophication), and hydrologic modifications (water withdrawal, reservoir construction). Here, we review recent studies revealing that regional and global climatic change may benefit various species of harmful cyanobacteria by increasing their growth rates, dominance, persistence, geographic distributions and activity. Future climatic change scenarios predict rising temperatures, enhanced vertical stratification of aquatic ecosystems, and alterations in seasonal and interannual weather patterns (including droughts, storms, floods); these changes all favour harmful cyanobacterial blooms in eutrophic waters. Therefore, current mitigation and water management strategies, which are largely based on nutrient input and hydrologic controls, must also accommodate the environmental effects of global warming.

Climate change: A catalyst for global expansion of harmful cyanobacterial blooms

Cyanobacteria are the Earth’s oldest oxygenic photoautotrophs and have had major impacts on shaping its biosphere. Their long evolutionary history (∼3.5 by) has enabled them to adapt to geochemical and climatic changes, and more recently anthropogenic modifications of aquatic environments, including nutrient over-enrichment (eutrophication), water diversions, withdrawals, and salinization. Many cyanobacterial genera exhibit optimal growth rates and bloom potentials at relatively high water temperatures; hence global warming plays a key role in their expansion and persistence. Bloom-forming cyanobacterial taxa can be harmful from environmental, organismal, and human health perspectives by outcompeting beneficial phytoplankton, depleting oxygen upon bloom senescence, and producing a variety of toxic secondary metabolites (e.g., cyanotoxins). How environmental factors impact cyanotoxin production is the subject of ongoing research, but nutrient (N, P and trace metals) supply rates, light, temperature, oxidative stressors, interactions with other biota (bacteria, viruses and animal grazers), and most likely, the combined effects of these factors are all involved. Accordingly, strategies aimed at controlling and mitigating harmful blooms have focused on manipulating these dynamic factors. The applicability and feasibility of various controls and management approaches is discussed for natural waters and drinking water supplies. Strategies based on physical, chemical, and biological manipulations of specific factors show promise; however, a key underlying approach that should be considered in almost all instances is nutrient (both N and P) input reductions; which have been shown to effectively reduce cyanobacterial biomass, and therefore limit health risks and frequencies of hypoxic events.

Harmful cyanobacterial blooms: causes, consequences, and controls.

The cyanobacteria or "blue-green algae", as they are commonly termed, comprise a diverse group of oxygenic photosynthetic bacteria that inhabit a wide range of aquatic and terrestrial environments, and display incredible morphological diversity. Many aquatic, bloom-forming species of cyanobacteria are capable of producing biologically active secondary metabolites, which are highly toxic to humans and other animals. From a toxicological viewpoint, the cyanotoxins span four major classes: the neurotoxins, hepatotoxins, cytotoxins, and dermatoxins (irritant toxins). However, structurally they are quite diverse. Over the past decade, the biosynthesis pathways of the four major cyanotoxins: microcystin, nodularin, saxitoxin and cylindrospermopsin, have been genetically and biochemically elucidated. This review provides an overview of these biosynthesis pathways and additionally summarizes the chemistry and toxicology of these remarkable secondary metabolites.

https://www.mdpi.com/1660-3397/8/5/1650/pdf

On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin.

http://www.iopan.gda.pl/oceanologia/482mazur.pdf

Toxic Nodularia spumigena blooms in the coastal waters of the Gulf of Gdańsk: a ten-year survey*

http://agro.icm.edu.pl/agro/element/bwmeta1.element.agro-article-79cdf0df-e6db-43c7-a774-a723652ca99e/c/433mazur.pdf

Stability of cyanotoxins, microcystin-LR, microcystin-RR and nodularin in seawater and BG-11 medium of different salinity

Nodularin is a potent hepatotoxic cyclic pentapeptide produced by planktonic cyanobacterium Nodularia spumigena. Bloom and culture samples of the cyanobacterium collected and isolated from the Gulf of Gdansk, southern Baltic Sea, were analyzed. Hybrid quadrupole-time-of-flight liquid chromatography/mass spectrometry/mass spectrometry (TOF-LC/MS/MS) with ionspray (ISP) and collision-induced dissociation (CID) were used to characterize nodularin and its analogues. The identification process was based on the comparison of recorded product ion spectra with the previously reported FAB-MS/CID (high-energy) mass spectra of the corresponding nodularin variants. Amino acid structures and sequences were derived from the fragmentation pattern of the [M+H](+) ions. Apart from unmodified nodularin with an arginine residue (NOD-R), three demethylated variants have been found. The sites of demethylation were located on aspartic acid [Asp(1)]NOD, the Adda residue [DMAdda(3)]NOD, and dehydrobutyric acid [dhb(5)]NOD. In two other nodularin variants an additional methyl group is located in the Adda [MeAdda]NOD and Glu [Glu(4)(OMe)]NOD residues. The linear NOD and the geometrical isomer of NOD-R, reported earlier in N. spumigena from New Zealand, have also been detected. Two of the total eight nodularin variants characterized in the present study, [dhb(5)]NOD and [MeAdda]NOD, have not been described earlier.

Characterization of nodularin variants in Nodularia spumigena from the Baltic Sea using liquid chromatography/mass spectrometry/mass spectrometry

In the Gulf of Gdansk, as in other parts of the Baltic Sea, toxic blooms of Nodularia spumigena are an annual phenomenon. In the present work, the accumulation of nodularin (NOD), a cyanobacterial pentapeptide hepatotoxin, in sediments, blue mussels, and flounders from the Gulf of Gdansk was studied by enzyme-linked immunosorbent assay (ELISA). In the surface layers of the sediments NOD concentration ranged from 2.3 ng/g dry weight (dw) several months after cyanobacterial bloom to 75 ng/g dw during the bloom. The highest toxin content in mussels was 139 ng/g dw. In two sampling stations situated in the coastal waters of the Gulf of Gdansk the concentrations of NOD in sediments and mussels were significantly lower than those measured in the Gulf of Finland. In sediments and mussels collected in the Gulf of Gdansk, the toxin was also detected in March when N. spumigena did not occur. In flounder, NOD accumulated in the liver (489 ng/g dw), guts (21 ng/g dw), and gonads (21 ng/g dw). Hybride quadrupole-time-of-flight liquid chromatography/mass spectrometry/mass spectrometry (TOF-LC/MS/MS) confirmed the presence of NOD in sediment, mussel, and fish samples. Additionally, other NOD analogues, ([DMAdda3]NOD and [dhb5]NOD), were detected in sediments and mussel tissue. No NOD conjugates with reduced glutathione or cysteine were found in fish and mussels. © 2007 Wiley Periodicals, Inc. Environ Toxicol 22: 101–111, 2007.

https://onlinelibrary.wiley.com/doi/pdf/10.1002/tox.20239

Accumulation of nodularin in sediments, mussels, and fish from the Gulf of Gdańsk, southern Baltic Sea.

Culture experiments on the toxic Nodularia spumigena strain NSGG-1 isolated from the Gulf of Gdansk showed a significant effect of salinity on growth and nodularin production Growth of the NSGG-1 strain, was optimal between 7 and 18 psu, lower at 3 and 24 psu and was significantly inhibited at the extreme salinities of 0 and 35 psu Nodularin (NOD) content of N spumigena, estimated by the NOD/Chla ratios, correlated positively with salinity and increased from 0 to 35 psu The NOD/Chla ratio on day 10 of growth was high, and, reached the maximum at day 30 A sudden increase in salinity from 7 to 18 and 35 psu resulted in plasmolysis of Nodularia cells Salinity was also observed to have other effects on NSGG-1; the filaments were longest at 7 psu, while an increased number of akinetes were formed at 35 psu The number of heterocytes was markedly reduced at the extreme salinities This latter finding might explain why Nodularia blooms do not occur outside a certain salinity range in nitrogen-deficient waters

M. Plinski

Papers

Toxic Nodularia spumigena blooms in the coastal waters of the Gulf of Gdańsk: a ten-year survey*

Stability of cyanotoxins, microcystin-LR, microcystin-RR and nodularin in seawater and BG-11 medium of different salinity

Characterization of nodularin variants in Nodularia spumigena from the Baltic Sea using liquid chromatography/mass spectrometry/mass spectrometry

Accumulation of nodularin in sediments, mussels, and fish from the Gulf of Gdańsk, southern Baltic Sea.

The effect of salinity on the growth, toxin production, and morphology of Nodularia spumigena isolated from the Gulf of Gdańsk, southern Baltic Sea