The proliferation of Cyanobacterial blooms: A toxic blue tide

Dr Assaf Sukenik is Senior Scientist at Kinneret Limnological Laboratory of the Israel Oceanographic and Limnological Research. His research interests concern the physiology and biochemistry of freshwater and marine algae, Cyanobacteria and algal toxins, the water quality of freshwater ecosystems.

What are cyanobacteria and what is their natural habitat?

Cyanobacteria (from the Greek word κυανοσ =blue), also known as blue-green algae, constitute the largest, most diverse, and most widely distributed group of photosynthetic oxygenic (oxygen-evolving) prokaryotes^[1]. They acquire their energy through photosynthesis, thus are often referred to as algae, although their prokaryotic characteristics (for example, their DNA is not enclosed in a nucleus) differentiate them from eukaryotic^[2] algae. The blue-green colour of cyanobacteria is given by their suite of photosynthetic pigments, which differ from that of eukaryotic algae.

Cyanobacteria are also among the oldest organisms on Earth. They appear in fossil records, in sedimentary rocks deposited in shallow seas and lakes 3.5 billion years ago. They played a major role in raising the level of free oxygen in the atmosphere of early Earth and contributed to the evolution of plants. Sometime in the late Proterozoic, or in the early Cambrian, about half a billion years ago, cyanobacteria began to take up residence within certain eukaryotic cells, providing organic compounds for the eukaryotic host via photosynthesis in return for a home in a process known as endosymbiosis^[3].

Cyanobacteria are found in a diverse range of habitats, from freshwater to oceans, bare rocks, soils, hydrothermal springs and arctic or glacial environments. In aquatic ecosystems, cyanobacteria proliferate and create blooms under favourable conditions of high nutrient abundance, warm water, calm weather conditions, and the presence of light. In the temperate zone, cyanobacterial dominance is usually pronounced during late summer-fall. In tropical and subtropical regions, it can continue year-round.

Cyanobacterial blooms collapse, gradually or abruptly, due to exhaustion of nutrients, increased vertical mixing, cooler temperature, pathogens such as cyanophages and enhanced photo-oxidation due to the exposition of floating scum to strong light. The increasing frequency of cyanobacteria bloom events and the expanded geographical coverage of such blooms demonstrate the wide range of adaptive characteristics of this ancient group of organisms.

We often hear cyanobacteria referred to as “harmful algal bloom”. What is their impact on water quality?

Harmful Algal Blooms, or HABs, occur when photosynthetic organisms that live in the sea and freshwater habitats—grow out of control, causing a nuisance, due to the accumulation of high-density biomass in the water column and stagnant scum. HABs give rise to odour problems and present a health hazard for people, animals and birds, in the case of toxin-producing HAB species.

Cyanobacteria are key players in the global phenomenon of HAB. Over the last three decades, the intensification of cyanobacteria blooms (cyanoHABs) in diverse freshwater ecosystems has been reported worldwide (Figure 1). Several blooms of cyanobacteria are associated with the production of toxins that limit the use of water bodies as resources for drinking water and irrigation, perturbing their ecological stability and disturbing regional economies.

Figure 1. Cyanobacteria bloom events around the world. A) Thick scum of the cyanobacterium Microcystis aeruginosa accumulated against the wall of Hartbeespoort Dam, South Africa, mid-1980s [8]. B) A surface scum of Microcystis in Dianchi Lake, Kunming, China September 2015. The boats in the background are equipped with screening drums and harvest the biomass to be used for land fertilization. (Photo credit Sukenik) C) Cyanobacteria bloom in Lake Eerie, May 2017. (Photo source: NOAA)

CyanoHABs present a unique challenge to drinking water utilities, as the water treatment process should remove biomass of toxic cyanobacteria (particulate matter) as well as soluble toxins. Conventional water treatment process (flocculation and filtration) impose the release of cell-bound toxins: as the cyanobacteria cell barrier gets damaged, cell content, including toxins, leaks to the water increasing the concentration of soluble toxins. Consequently, complementary physical (adsorption by activated carbon or exclusion by membrane filtration), chemical and biological (oxidation, biological inactivation and UV) treatment processes are needed for the degradation and removal of soluble toxins.

How are they dangerous for human life?

Cyanobacteria can produce a variety of cyanotoxins such as microcystins, saxitoxins, nodularin, cylindrospermopsin, and anatoxin-a. These compounds are linked to a variety of deleterious health effects, from skin rashes to liver failure. Microcystins and nodularins, for example, are known as liver toxins whereas saxitoxins and anatoxin-a are potent neurotoxins. The major concern relates to the exposure of humans to cyanotoxins through drinking water, although other routes such as food, recreational waters, and nutritional supplements should be considered. The most dramatic event of human fatality due to exposure to cyanotoxins was reported in 1996 when dialysis patients were accidentally treated with cyanotoxins contaminated water [1]. A toxic bloom event that affected a large community occurred in the USA, in the late summer of 2014, when a large toxic cyanobacterial bloom shut down the drinking water supply of Toledo (Ohio) causing massive disruption in the city of over half a million inhabitants [2]. In China, more than 60 % of the lakes have undergone harmful cyanoHABs. The three largest shallow freshwater lakes, Taihu, Chaohu and Dianchi, frequently suffer from toxic cyanoHABs. In early summer of 2007, a massive accumulation of Microcystis biomass in Lake Taihu overwhelmed the drinking water plant and caused a drinking water crisis in Wuxi city, which affected more than 4 million people [3].

How are cyanobacteria monitored?

Monitoring of water bodies includes physical-chemical and biological parameters. Monitoring of cyanobacteria population calls for sample collection and microscopic observation and enumeration of phytoplankton species in water samples (Figure 2).

Figure 2. Dr Sukenik and co-workers collect samples of surface scum in Lake Kinneret (Sea of Galilee, Israel) during a Microcystis bloom event, February 2013. (photo credit Dr. Ilia Ostrovsky Kinneret Limnological Laboratory IOLR)

Identification and quantification of cyanotoxins in the water require advanced chemical techniques. In both cases, alternative indirect methods have been developed and implemented for real-time (or near real-time) monitoring of cyanobacteria such as in situ flow-through or submersible fluorometer and satellite remote sensing (Figure 3) [4]. For quantification of cyanotoxins, specific immunological techniques were established and are now widely used for preliminary evaluation and early warning in the case of toxic blooms [4].

Figure 3. Satellite remote sensing of cyanobacteria blooms in Lake Kinneret, Sea of Galilee, Israel (above) and Taihu Lake, China (below). Lake Kinneret – Left: A satellite (Landset TM 8) image showing green patches of cyanobacteria during a bloom event of Microcystis, February 2016. Right: False-colour image present chlorophyll surface density derived from the satellite image (courtesy: Dr G. Tibor, Israel Oceanographic & Limnological Research). Taihu Lake – Left: An Image of the satellite sensor GOCI (Geostationary Ocean Color Image) showing a cyanobacteria bloom (surface scum) in Taihu Lake, China on 27 November 2015. Right: False-colour Red-Green-Blue image presents equivalent surface cyanobacteria density derived from the GOCI image [7].

Cyanobacteria tend to dominate water bodies of all types, especially if they are eutrophic^[4] [5]. High phytoplankton density leads to high turbidity and low light intensity in the water column, conditions under which cyanobacteria have competitive advantages. Various cyanobacteria have unique physiological traits that provide an ecological advantage, such as fixation of atmospheric nitrogen under the limitation of inorganic nitrogen, CO₂ concentrating mechanisms, efficient phosphate assimilation, buoyancy regulation and wide range of temperature tolerance. Their proliferation is further enhanced, as many of the colonial and filamentous cyanobacteria are not grazed by crustacean zooplankton. Because of their positive buoyancy, many species of cyanobacteria float through stable layers of water and accumulate at the surface where they form scum. This surface accumulation gives cyanobacteria access to CO₂ and light, and at the same time, they shade the water column, so less light penetrates underneath the water. Under the same stable conditions, most other algae sink. Thus, by competitive exclusion, blooming cyanobacteria tend to dominate the phytoplankton community.

Is there any connection between cyanobacteria proliferation and human activities?

The proliferation of cyanobacteria in many aquatic ecosystems, their invasion into new sites and their bloom extension over time are likely to expand further in coming decades owing to continued eutrophication, rising atmospheric CO₂ concentrations and global warming. These driving forces are interconnected and strongly influenced by human activities.

What can we expect in the near future, in relation to climate change?

Given the physiological traits of cyanobacteria that enable them to thrive and proliferate under the current and regional eutrophication and climate change, further global expansion of cyanobacteria blooms is expected. Bloom events and the persistence of blooms are predicted to increase as long as these global environmental processes continue [6]. In order to prevent or suppress cyanobacterial blooms under the current climate trend, two general strategies have been proposed. One strategy calls for management of nutrients by reducing loads from external and internal sources thereby controlling the intensity and duration of the blooms; The other strategy is treating the blooming population in situ by hydrological manipulations or by application of algaecides, thus selectively reducing the cyanobacteria population. Despite intense efforts to limit toxic blooms, persistence and reappearance of cyanobacteria blooms are expected worldwide.

References

1. Azevedo SM, Carmichael WW, Jochimsen EM, Rinehart KL, Lau S, Shaw GR, Eaglesham GK. (2002) Human intoxication by microcystins during renal dialysis treatment in Caruaru—Brazil. Toxicology. 181:441-6. https://doi.org/10.1016/S0300-483X(02)00491-2
2. Steffen MM, Davis TW, McKay RM, Bullerjahn GS, Krausfeldt LE, Stough JM, Neitzey ML, Gilbert NE, Boyer GL, Johengen TH, Gossiaux DC. (2017) Ecophysiological examination of the Lake Erie Microcystis bloom in 2014: linkages between biology and the water supply shutdown of Toledo, OH. Environmental science & Technology. 51:6745-55. https://doi.org/10.1021/acs.est.7b00856
3. Qin B, Zhu G, Gao G, Zhang Y, Li W, Paerl HW, Carmichael WW. (2010) A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environmental management. 45:105-12. https://doi.org/10.1007/s00267-009-9393-6
4. Zamyadi A, Choo F, Newcombe G, Stuetz R, Henderson RK. (2016) A review of monitoring technologies for real-time management of cyanobacteria: Recent advances and future direction. Trends in Analytical Chemistry.85:83-96. https://doi.org/10.1016/j.trac.2016.06.023
5. Codd GA. (2000) Cyanobacterial toxins, the perception of water quality, and the prioritisation of eutrophication control. Ecological engineering. 16:51-60. https://doi.org/10.1016/S0925-8574(00)00089-6
6. Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JM, Visser PM. (2018) Cyanobacterial blooms. Nature Reviews Microbiology. 16: 471–483. https://doi.org/10.1038/s41579-018-0040-1
7. Qi L, Hu C, Visser PM, Ma R. (2018) Diurnal changes of cyanobacteria blooms in Taihu Lake as derived from GOCI observations. Limnology and Oceanography. 63:1711-26. https://doi.org/10.1002/lno.10802
8. Sukenik A, Zohary T and Padisák J. (2009) Cyanoprokaryota and Other Prokaryotic Algae. In: Gene E. Likens, (Editor) Encyclopedia of Inland Waters. volume 1, pp. 138-148 Oxford: Elsevier.

^[1] Prokaryotes are organisms that have a simple cell structure without compartmentalisation and their cells lack a nucleus. They belong to the kingdom Monera that is further classified into two domains: Archaebacteria and Eubacteria (including cyanobacteria).

^[2] Eukaryotes are organisms whose cells have a nucleus enclosed within membranes. Eukaryotic cells contain other membrane-bound organelles such as mitochondria and the Golgi apparatus. Cells of plants and algae contain chloroplasts. Eukaryotes may be multicellular and include organisms consisting of many cell types forming different kinds of tissue.

^[3] Endosymbiosis – An evolutionary process considered responsible for the evolvement of eukaryotic cells. Early prokaryotes were engulfed by other cells via phagocytosis. The engulfed prokaryotic cell remained undigested as it contributed new functionality to the engulfing cell (e.g. photosynthesis -chloroplast, oxygenic respiration -mitochondria). Over generations, the engulfed cell lost some of its independent utility and became a supplemental organelle.

^[4] rich in nutrients thus supporting a dense phytoplankton population