Among the bloom-forming cyanobacteria, Microcystis aeruginosa is one of the mostharmful species. The prevalence of toxic species and their toxicity profiles vary each yeardepending on environmental variables, despite their dynamics being not well understood.Imbalances in nutrient concentrations, the greater frequency and intensity of higher averagetemperatures and less severe winters, and the alternation between periods of positive andnegative precipitation anomalies were identified as conditions favoring the prevalence of M.aeruginosa. Similarly, dry periods (corresponding to a prevailing La Niña condition) wereeven more conducive to the formation of harmful algal blooms of pronounced intensity.Moreover, toxin production is temperature-dependent and some strains are capable ofproducing multiple microsystins (MCs). Thus, the role of environmental variables incontrolling the genetic expression of toxin synthetase of individual toxin-producing genesis still unknown.Fil: Giannuzzi, Leda. Universidad Nacional de La Plata; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata; ArgentinaFil: Hernando, Marcelo Pablo. Red de Investigación de Estresores Marinos-costeros En América Latina y El Caribe; Argentina. Comisión Nacional de Energía Atómica; Argentin

Giannuzzi, Leda

Hernando, Marcelo Pablo

Microorganisms

English

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Citation: Giannuzzi, L.; Hernando,M. The Eco-Physiological Role ofMicrocystis aeruginosa in a ChangingWorld. Microorganisms 2022, 10, 685.https://doi.org/10.3390/microorganisms10040685Received: 16 March 2022Accepted: 19 March 2022Published: 23 March 2022Publisher’s Note: MDPI stays neutralwith regard to jurisdictional claims inpublished maps and institutional affil-iations.Copyright: © 2022 by the authors.Licensee MDPI, Basel, Switzerland.This article is an open access articledistributed under the terms andconditions of the Creative CommonsAttribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).microorganismsEditorialThe Eco-Physiological Role of Microcystis aeruginosa in aChanging WorldLeda Giannuzzi 1 and Marcelo Hernando 2,3,*1 Area of Toxicology, School of Exact Sciences, National University of La Plata (UNLP),La Plata 1900, Argentina; leda@biol.unlp.edu.ar2 Department of Radiobiology, National Atomic Energy Commission, San Martin 1650, Argentina3 Red de Investigación de Estresores Marinos-costeros en América Latina y el Caribe (REMARCO),Mar del Plata 7602, Argentina* Correspondence: mhernando@cnea.gov.ar1. IntroductionAmong the bloom-forming cyanobacteria, Microcystis aeruginosa is one of the mostharmful species. The prevalence of toxic species and their toxicity profiles vary each yeardepending on environmental variables, despite their dynamics being not well understood.Imbalances in nutrient concentrations, the greater frequency and intensity of higher averagetemperatures and less severe winters, and the alternation between periods of positive andnegative precipitation anomalies were identified as conditions favoring the prevalence of M.aeruginosa. Similarly, dry periods (corresponding to a prevailing La Niña condition) wereeven more conducive to the formation of harmful algal blooms of pronounced intensity.Moreover, toxin production is temperature-dependent and some strains are capable ofproducing multiple microsystins (MCs). Thus, the role of environmental variables incontrolling the genetic expression of toxin synthetase of individual toxin-producing genesis still unknown.2. Increased Temperature and Solar Ultraviolet Effects (UVR)Great efforts have been put to assess the impact on diverse organisms of both UVR andglobal warming due to the input of greenhouse gas. Solar ultraviolet A (UVA) radiation(315–400 nm) has also been implicated in the inhibition of primary production and plays anadditional role in activating UV-damage-repair mechanisms. UVR is currently considereda stressor for aquatic organisms even under its normal levels, and for cyanobacteria inparticular. Very little is known about the interactive effects of UVR and temperature thatmay act synergic or antagonistically [1]. Higher temperature increases growth rate ofcyanobacteria by accelerating metabolism, while at the ecosystem level it favors thermalstratification that promotes biomass accumulation at the water surface [2]. Global warmingincreases water temperatures and thus the stratification of water bodies depending ontheir morphometry and wind speed. By reducing the thickness of the upper mixed layer,organisms are exposed to a higher dose of UVR with physiological consequences likeincreased reactive oxygen/nitrogen species, lipid damage, and antioxidant protection [1].2.1. Fatty Acids (FAs) CompositionThe study by de la Rosa et al. [3] demonstrated differential sensitivity of omega 3 (ω3)fatty acids (FAs) in M. aeruginosa after two days of exposure to elevated temperature (29 ◦C)compared with the control (26 ◦C). Thus, although no significant differences were found inunsaturated/saturated FAs, differential sensitivity ofω3 versusω6 was observed at 29 ◦C.Previous studies have shown that UVR can affect FAs in cyanobacteria by damag-ing cell integrity, including oxidative damage to unsaturated or polyunsaturated lipids.According to [1], the lower lipid peroxidation of selected unsaturated fatty acids (UFAs)Microorganisms 2022, 10, 685. https://doi.org/10.3390/microorganisms10040685 https://www.mdpi.com/journal/microorganismsMicroorganisms 2022, 10, 685 2 of 4and the high capacity of scavenger systems could probably explain the high adaptabilityof M. aeruginosa to high UVR stress at high temperatures. It was evident that selectedpolyunsaturated fatty acids (PUFAs) (mainly ω6) play an important role in adaptationto high temperatures, in addition to the increased activity of enzymatic antioxidants thatshifts temperature growth from 26 to 29 ◦C.2.2. MicrocystinDziallas and Grossart [4] hypothesized that MCs function as radical scavengers. More-over, several studies showed increased sensitivity of MC-deficient mutants under highlight and oxidative stress conditions, supporting the hypothesis of an antioxidant functionof MC. Giannuzzi et al. [2] showed a decreased rate of several MCs (D-Leu1; Leu1, A sp3;Leu1, Glu(OCH3)6; M(O)1) after several days of exposure to high temperatures (29 ◦C).Recently, Malanga et al. [5] showed effective antioxidant activity for [D-Leu1] MC-LRagainst water-soluble radicals in the first in vitro results related to the role of MC as anantioxidant. These results confirm the suggestions of the above authors regarding thedecrease in the concentration of MC under environmental conditions requiring adaptationof M. aeruginosa. However, Giannuzzi et al. [2] also demonstrated a significant increase inone of the MCs produced by M. aeruginosa. This was the case for MC-LR, one of the mostpotent toxins in the world, when cultures were exposed to elevated temperature (29 ◦C).This suggests that the antioxidant function of the different MCs needs further investigation.Regarding UVR exposure, Hernando et al. [6] also showed that short-term exposure(4 h) of M. aeruginosa to UVA resulted in a significant decrease in [Leu1] MC-LR (p < 0.05)when UVR + photosynthetic available radiation (PAR) doses reached 11,173 kJ m−2(a UVBR dose of 74.4 kJ m−2).3. Microcystin Brain ToxicityMCs are potent hepatotoxins and tumor promoters that utilize an active carrier mecha-nism in the liver, considered one of the most dangerous toxins groups worldwide and beingthe leading cause of human fatalities. Despite the large amount of information available,interest in MCs continues to grow, as they are known to pose a threat to livestock, fisheries,aquaculture, human health, and wildlife through exposure via drinking, environmental,and recreational waters.Although most studies to date have focused on the effects of MC on the liver, few stud-ies have evaluated potential effects on the brain. A group of experts has called for studieson toxicity to neurodevelopment to be conducted for all major groups of cyanotoxins, asthis topic remains largely unexploredMoreover, in mammals, MCs exhibit potent neurotoxic activity that can cause signifi-cant behavioral changes, loss of neurons, and severe morphological changes, and on theother hand, they induce oxidative stress at the brain level and changes in the neuronalcytoskeleton. Effects such as memory loss after exposure to MC-LR are also highlighted [7].In addition, ultrastructural brain changes have been observed in rats brains after exposureto MC-LR (10 µg/kg body weight/day) during gestation and lactation [8]. Histological andultrastructural lesions and severe oxidative damage were also observed in the hippocampustreated with MC-LR (10 µg/L per 1µL) [9]. Recently, evaluating the chronic effects of MCin rats, it has been determined that MC-LR and D-Leu1 MC-LR do not reach the samebrain structures, with the hippocampus being the area most affected by D-Leu1 MC-LR(Hernando, personal communication).4. Microcystin Depuration ImprovesPhysicochemical control methods include UVR, ultrasound, and algaecides such ascopper sulphate and chlorination. However, these measures are rarely applied on a largescale due to their high cost and potential secondary pollution. Therefore, the developmentof environmentally friendly and economical methods to control harmful algae blooms(HABs) is of both theoretical and practical importance. The release and degradation ofMicroorganisms 2022, 10, 685 3 of 4MC-LR, produced by M. aeruginosa during the flocculation and lysis phases, have alsobeen studied because of its importance in controlling and treating HABs without causingadverse effects.Great efforts are currently being made to implement new, more advanced measuresto eliminate cyanobacteria and toxins in a water treatment plant. Conventional treatmentapproaches such as coagulation/flocculation of cells by physical retention or chemicaloxidation employing chemical compounds such as aluminum polychloride present variouspractical, economic or environmental disadvantages. A new emerging technologies, suchas advanced oxidation processes (AOPs), new materials, such as activated carbon, chitosanand others, have great potential to resolve this issue. However, their efficiency, applica-bility, economic, practical and environmental aspects must be studied in depth. Finally, acombination of different treatment methods, including a multi-barrier approach, needs tobe considered to produce drinking water.5. Conclusions and Future RemarksConsidering the importance of water bodies where recurrent blooms of M. aeruginosaoccur, it is essential to understand the relationship between environmental variables and thetoxicity in them for the management and implementation of prevention measures relatedto the distribution and consumption of drinking water. Cyanobacteria were able to developdiverse and highly effective eco-physiological adaptations and strategies for ensuringsurvival and dominance in aquatic environments undergoing natural and human-inducedenvironmental change. Thus, changes in metabolism and physiology may have seriousconsequences over the entire ecosystem. Considering that MCs are chemically very stable,and the rapid chemical modification of its structure or its antioxidant function againstvarious environmental changes, these toxins can finally end up in human food throughthe food chain or drinking water, and the chronic impact of accumulated MCs on humanhealth cannot be ignored; not only on the liver, but also in the brain, depending on theMC family as a function of the pre-exposure of M. aeruginosa to changing environmentalvariables. Other mechanisms of adaptation to changes in environmental variables may alsobe related to the composition of the cell lipid membrane. Shifts in FAs composition in afood web due to cyanobacterial blooms could potentially affect zooplankton/fish healthby altering their metabolic processes, a pathway that is only recently being explored introphic ecology.This issue summarizes the current knowledge of M. aeruginosa, focusing on physiology,toxin production, toxic effects and depuration methods. It discusses how these factorsinfluence the ecology of this globally important cyanobacterium, identifies a number ofgaps in our knowledge, and provides a list of high-priority research topics. The aim of theSpecial Issue on M. aeruginosa is to establish how, and to what extent if any, changes inenvironmental conditions can influence the global dominance of cyanobacteria.Funding: This study was financially supported by the National University of La Plata (UNLP X862)and project RLA7025 “Strengthening Capacities in Marine and Coastal Environments Using Nuclearand Isotopic Techniques” from IAEA.Institutional Review Board Statement: Not applicable.Informed Consent Statement: Not applicable.Data Availability Statement: We choose to exclude this statement due the study did not report any data.Conflicts of Interest: The authors declare no conflict of interest.References1. De la Rosa, F.; De Troch, M.; Malanga, G.; Marcelo, M.H. Physiological responses and specific fatty acids composition of Microcystisaeruginosa exposed to total solar radiation and increased temperature. Photochem. Photobiol. Sci. 2021, 20, 805–821. [CrossRef][PubMed]Microorganisms 2022, 10, 685 4 of 42. Giannuzzi, L.; Krock, B.; Minaglia, M.; Rosso, L.; Houghton, C.; Sedan, D.; Hernando, M. Growth, toxin production, active oxygenspecies and catalase activity of Microcystis aeruginosa (Cyanophyceae) exposed to temperature stress. Comp. Biochem. Physiol.Part C Toxicol. Pharmacol. 2016, 189, 22–30. [CrossRef] [PubMed]3. De la Rosa, F.; De Troch, M.; Malanga, G.; Hernando, M. Differential sensitivity of fatty acids and physiological responses ofMicrocystis aeruginosa (Cyanobacteria) exposed to increased temperature. Comp. Biochem. Physiol. Part C 2020, 235, 108773.4. Dziallas, C.; Grossart, H. Increasing oxygen radicals and water temperature select for toxic Microcystis sp. PLoS ONE 2011,6, e25569. [CrossRef] [PubMed]5. Malanga, F.; Giannuzzi, L.; Hernando, M. The possible role of microcystin (D-Leu1 MC-LR) as an antioxidant on Microcystisaeruginosa (Cyanophyceae). In vitro and in vivo evidence. Comp. Biochem. Physiol. Part C 2019, 225, 108575. [CrossRef] [PubMed]6. Hernando, M.; Crettaz Minaglia, M.; Malanga, G.; Houghton, C.; Andrinolo, D.; Sedan, D.; Rosso, L.; Giannuzzi, L. Physiologicalresponses and toxin production of Microcystis aeruginosa in short term exposure to solar UV radiation. Photochem. Photobiol. Sci.2018, 17, 69–80. [CrossRef] [PubMed]7. Maidana, M.; Carlis, V.; Galhardi, F.; Yunes, J.; Geracitano, L.; Monserrat, J.; Barros, D. Effects of microcystins over short-andlong-term memory and oxidative stress generation in hippocampus of rats. Chem.-Biol. Interact. 2006, 159, 223–234. [CrossRef][PubMed]8. Zhao, S.; Li, G.; Chen, J. A proteomic analysis of prenatal transfer of microcystin-LR induced neurotoxicity in rat offspring. J.Proteom. 2015, 114, 197–213. [CrossRef] [PubMed]9. Li, W.; Chen, J.; Xie, P.; He, J.; Guo, X.; Tuo, X.; Zhang, W.; Wu, L. Rapid conversion and reversible conjugation of glutathionedetoxification of microcystins in bighead carp (Aristichthys nobilis). Aquat. Toxicol. 2014, 147, 18–25. [CrossRef] [PubMed]

The Eco-Physiological Role of Microcystis aeruginosa in a Changing World

Among the bloom-forming cyanobacteria, Microcystis aeruginosa is one of the most harmful species [...

Leda Giannuzzi

Marcelo Hernando

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The Eco-Physiological Role of <i>Microcystis aeruginosa</i> in a Changing World

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The Eco-Physiological Role of Microcystis aeruginosa in a Changing World

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