Cyanobacterial Harmful Algal Blooms in Aquatic Ecosystems: a Comprehensive Outlook on Current and Emerging Mitigation and Control Approaches
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microorganisms Review Cyanobacterial Harmful Algal Blooms in Aquatic Ecosystems: A Comprehensive Outlook on Current and Emerging Mitigation and Control Approaches Assaf Sukenik 1,* and Aaron Kaplan 2 1 The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, P.O. Box 447, Migdal 14950, Israel 2 Department of Plant and Environmental Sciences, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Givat Ram, Jerusalem 9190401, Israel; [email protected] * Correspondence: [email protected]; Tel.: +972-4-900-8233 Abstract: An intensification of toxic cyanobacteria blooms has occurred over the last three decades, severely affecting coastal and lake water quality in many parts of the world. Extensive research is being conducted in an attempt to gain a better understanding of the driving forces that alter the ecological balance in water bodies and of the biological role of the secondary metabolites, toxins included, produced by the cyanobacteria. In the long-term, such knowledge may help to develop the needed procedures to restore the phytoplankton community to the pre-toxic blooms era. In the short-term, the mission of the scientific community is to develop novel approaches to mitigate the blooms and thereby restore the ability of affected communities to enjoy coastal and lake waters. Here, we critically review some of the recently proposed, currently leading, and potentially emerging Citation: Sukenik, A.; Kaplan, A. mitigation approaches in-lake novel methodologies and applications relevant to drinking-water Cyanobacterial Harmful Algal treatment. Blooms in Aquatic Ecosystems: A Comprehensive Outlook on Current Keywords: cyanobacteria; harmful bloom; bloom prevention; oxidative stress; water treatment and Emerging Mitigation and Control Approaches. Microorganisms 2021, 9, 1472. https://doi.org/10.3390/ microorganisms9071472 1. Introduction Academic Editor: Konstantinos Cyanobacteria (also known as Cyanophyta, Cyanoprokaryota, Chloroxybacteria, and Ar. Kormas blue-green algae) constitute the largest, most diverse, and most widely distributed group of photosynthetic organisms. They were the first to perform oxygenic photosynthesis, splitting Received: 10 June 2021 the water molecule and providing O2 to the atmosphere. Accordingly, they played a major Accepted: 6 July 2021 role in many biogeochemical processes that revolutionary impacted the biosphere [1–3], Published: 9 July 2021 including nutrient availability and the development of heterotrophs and O2-consuming organisms. Presently, cyanobacteria are important primary producers contributing to the Publisher’s Note: MDPI stays neutral plankton, benthos, epiphyton, and epilithon in various aquatic and terrestrial ecosystems. with regard to jurisdictional claims in Over the last few decades, they have become mostly known for their notorious blooms in published maps and institutional affil- various water bodies. The bloom-forming genera Microcystis, Anabaena (Dolichospermum), iations. Aphanizomenon, Cylindrospermopsis, and Lyngbya often dominate the spring–fall assemblages in water bodies. This is being attributed to global warming and anthropogenic activities leading to eutrophication. Cyanobacteria proliferate under favorable conditions of nutrient abundance, warm Copyright: © 2021 by the authors. water temperature, calm weather conditions, and the presence of light, often to the extent Licensee MDPI, Basel, Switzerland. of forming a bloom. The ability of many toxic strains to optimize their location in the water This article is an open access article column is a meaningful ecological advantage. This is accomplished through buoyancy distributed under the terms and regulation, which is determined by the balance between gas vesicles inflation and the conditions of the Creative Commons ballast [4]. Consequently, many species of planktonic cyanobacteria accumulate at the Attribution (CC BY) license (https:// surface, particularly in the morning after consuming a significant portion of their reserve creativecommons.org/licenses/by/ carbohydrates during the dark, and form floating scums. This surface accumulation 4.0/). Microorganisms 2021, 9, 1472. https://doi.org/10.3390/microorganisms9071472 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 25 Microorganisms 2021, 9, 1472 2 of 24 face, particularly in the morning after consuming a significant portion of their reserve car- bohydrates during the dark, and form floating scums. This surface accumulation provide the cyanobacteria with better access to CO2 and light while, at the same time, shading the provide the cyanobacteria with better access to CO2 and light while, at the same time, watershading column the water below. column In addition, below. allelopathy In addition, and allelopathy competitive and exclusion competitive support exclusion cyano- bacteriasupport blooms cyanobacteria and the blooms domination and the of dominationthe planktonic of thealgal planktonic assemblage algal [5]. assemblage The prolifera- [5]. tionThe of proliferation toxic cyanobacteria of toxic cyanobacteriais further augmented is further by augmentedlow grazing bypressure. low grazing Blooms pressure. of cya- nobacteriaBlooms of cyanobacteriaare undesirable are due undesirable to the accumulation due to the accumulationand rotting of and stagnant rotting biomass, of stagnant re- sultingbiomass, inresulting taste and in odor taste problems. and odor problems.More importantly, More importantly, as many species as many produce species an produce array ofan toxins, array of cyanobacteria toxins, cyanobacteria blooms constitute blooms constitute a serious a health serious hazard health referred hazard referred to as cyano- to as bacterialcyanobacterial harmful harmful algal algalblooms blooms (cyanoHAB (cyanoHABs).s). This Thishas attracted has attracted the attention the attention of both of both re- gionalregional and and national national water water and and nature nature authorities authorities,, as well as well as the as the general general public public affected affected by cyanoHABs.by cyanoHABs. TThoughhough cyanoHAB cyanoHABss and their environmental, health health,, and social consequences have been reviewed duringduring thethe lastlast threethree decades decades and and recently recently updated updated [6 –[68–],8], it isit imperativeis imperative to tocritically critically review review current current and and emerging emerging approaches approaches to mitigate to mitigate and controland control cyanoHABs, cyanoHABs, their theirecological ecological impact, impact and their, and effect their oneffect consumers on consumers via drinking via drinking water or water recreational or recreational activities. activities.Here, we Here focus, we on focus three on domains three domains that cover that thecover main the levelsmain levels of cyanoHAB of cyanoHAB treatment treat- mentand control: and control: the prevention the prevention of bloom of bloom development, development, in lake/reservoir in lake/reservoir treatment, treatment, and and in indrinking/potable drinking/potable water water treatment treatment (Figure (Figure1). 1). We We do do not not wish wish to provide to provide a comprehensive a comprehen- sivereview review for each for each component; component instead,; instead, we critically we critically evaluate evaluate the methodologies the methodologies currently cur- rentlyproposed proposed to mitigate, to mitigate, eliminate, eliminate and control, and control toxic cyanobacteria toxic cyanobacteria blooms, blooms as well, as as possible well as possiblefuture developments. future developments. Figure 1. Schematic presentation of strategies and techniques implemented to prevent the development of cyanoHAB and to mitigate potential impacts on aquatic ecosystemecosystem andand potablepotable water.water. 2. Prevention Prevention of of Bloom Bloom Development Development 2.1. Early Detection 2.1. Early Detection Naturally, reliable and sensitive approaches capable of the early detection of cyanoHABs Naturally, reliable and sensitive approaches capable of the early detection of cyano- are vital for their effective mitigation. A comprehensive analysis of the methodologies used HABs are vital for their effective mitigation. A comprehensive analysis of the methodolo- for monitoring biotic and abiotic parameters is beyond the scope of the present paper as they giesdiffer used substantially, for monitoring mainly biotic due and to the abiotic size of parameters the water bodyis beyond (for a the detailed scope review, of the present see [9]). paperNevertheless, as they differ it is worth substantially, mentioning mainly that amongdue to the size wide of range the water of monitoring body (for techniques a detailed reviewand devices, see [9]). used Nevertheless, by water authorities it is worth and managersmentioning of waterthat among bodies, the fluorescence wide range probes of mon- are itoringhighly effectivetechniques because and devices they allow used for by the water real-time authorities continuous and monitoringmanagers of of water cyanobacteria bodies, and algae. The deployment of such water quality monitoring systems with multi-sensor probes in tandem with fluorescence devices allows one to follow temporal variations to be Microorganisms 2021, 9, 1472 3 of 24 monitored using the concentration of chlorophyll and accessory pigments as surrogates for phytoplankton, including cyanobacteria in water [10,11]. In addition, very fast progress is