Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1
Daniela de Figueiredo
 -- 1375 2024-01-16 10:38:11 |
2 format correct
Catherine Yang
 Meta information modification 1375 2024-01-18 02:36:53 |

Video Upload Options

Do you have a full video?
Send video materials Upload full video

Confirm

Are you sure to Delete?
Yes No
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
De Figueiredo, D.R. Harmful Cyanobacterial Blooms. Encyclopedia. Available online: https://encyclopedia.pub/entry/53885 (accessed on 22 May 2024).
De Figueiredo DR. Harmful Cyanobacterial Blooms. Encyclopedia. Available at: https://encyclopedia.pub/entry/53885. Accessed May 22, 2024.
De Figueiredo, Daniela R.. "Harmful Cyanobacterial Blooms" Encyclopedia, https://encyclopedia.pub/entry/53885 (accessed May 22, 2024).
De Figueiredo, D.R. (2024, January 16). Harmful Cyanobacterial Blooms. In Encyclopedia. https://encyclopedia.pub/entry/53885
De Figueiredo, Daniela R.. "Harmful Cyanobacterial Blooms." Encyclopedia. Web. 16 January, 2024.
Harmful Cyanobacterial Blooms
Edit
This entry is adapted from the peer-reviewed paper 10.3390/hydrobiology3010002

Under the Climate Change scenario, the occurrence of Harmful Cyanobacterial Blooms (HCBs) is an increasingly concerning problem. Particularly for inland freshwaters, that have human populations depending on them for consumption or recreation, HCBs can lead to serious ecological damages and socio-economic impacts, but also to health risks for local communities. 

cyanobacterial blooms freshwaters remote sensing

1. Introduction

Cyanobacteria are ancient photoautotrophic bacteria, and their occurrence is ubiquitous throughout aquatic bodies, although they can also be found in terrestrial ecosystems or in symbiosis with other organisms, or even in extreme environments such as in hypersaline lakes, hot springs, polar regions, and deserts [1][2][3][4]. However, in freshwaters, the study of the cyanobacterial community has been the focus of particular interest due to the occurrence of Harmful Cyanobacterial Blooms (HCBs), resulting from the massive growth of cyanobacteria that are potentially toxic, with impacts on both aquatic and terrestrial organisms, leading to serious health impacts or even death [5][6][7][8][9][10][11][12][13][14][15][16]. Moreover, under a climate change scenario, the concern with HCBs is growing due to their spread and increased persistence worldwide [17][18][19][20][21][22], with major changes on the ecosystems [8][13][23][24] but also posing risks to human health [5][25][26] and leading to socio-economic impacts in local communities [18][27][28][29][30][31][32].
In fact, many bloom-forming cyanobacteria have been reported as toxic, with the production of a wide range of toxins generally classified into hepatotoxins, neurotoxins, cytotoxins and dermatotoxins/irritant toxins [26][33][34]. Nevertheless, the list of new cyanotoxins is still increasing [11][14][35][36]. The most reported cyanotoxins include: microcystins and nodularin (hepatotoxins); saxitoxins, anatoxins and β-methylamino-l-alanine (neurotoxins); cylindrospermopsin (cytotoxin); lyngbyatoxins and aplysiatoxins (dermatotoxins); and lipopolysaccharides (irritant toxins) [14][15][22][37][38][39][40]. For a long time, most attention has been given to microcystins, mainly due to its global spread occurrence and impacts on human health, either by acute or chronic exposure [5][39][41][42][43][44]. However, neurotoxic saxitoxins and anatoxin-a also pose significant health risks due to their rapid and acute poisonings [39][45][46] as well as the potential for chronic effects by extended exposure to low doses [47]. Cylindrospermopsin is another very frequent cyanotoxin [48][49], responsible for cytotoxic [26] and neurotoxic effects [50][51]. In fact, the proposed guideline value for long-term exposure to cylindrospermopsin in drinking water is 0.7 μg/L, which is even lower than the same guideline for microcystins (1.0 μg/L) [52]. Additionally, both hepatotoxins and neurotoxins can persist in water for long periods of time (from days up to several weeks) until its degradation [26][53], which increases the concern for extended exposure. The bioaccumulation of these toxins has also been addressed for aquatic organisms such as molluscs and fish [49][54][55][56][57] but also for crops irrigated with contaminated water [12][35][58][59][60], highlighting the risk range and potentially wider effects of cyanotoxins’ occurrence. The most common exposure routes to cyanotoxins include the consumption/drinking of contaminated water, but recreational exposure can also occur through the accidental water swallowing, skin contact or even inhalation of scum aerosols [33][45][61][62].

2. Impact of Intraspecific Variability on Blooms’ Ecology and Toxicity

2.1. Classical Taxonomy vs. Phylogenetic Approaches

Most historical records and ecological studies concerning cyanobacterial blooms have been based on the identification of bloom-forming cyanobacteria using classical taxonomy mainly sustained by phenotypic features, which can be tricky due to several reasons, namely the diversity of strains/ecotypes [63]. Moreover, with the rise of DNA-based molecular approaches (using mostly 16S rRNA gene sequences), the polyphyletic nature of some genera has become controversial [64][65][66][67] and several taxonomical revisions have been made for several species and even genera [63][68][69][70][71][72][73], using polyphasic approaches to integrate morphological, biochemical and molecular information [69][71][73]. This re-classification into new genera and species also amplified the confusion regarding the taxonomy of blooming cyanobacteria and their correct identification, particularly for Nostocaceae genera such as Anabaena and Aphanizomenon, which were divided into new genera including Dolichospermum, Chrysosporum, Cuspidothrix or Sphaerospermopsis [67][73][74][75]. For instance, Sphaerospermopsis aphanizomenoides was formerly known as Aphanizomenon aphanizomenoides (Forti) Horecká and Komárek and Anabaena aphanizomenoides Forti [68][69][73][76]. Other examples can be Raphidiopsis raciborskii and Cuspidothrix issatschenkoi, which were formerly known as Cylindrospermopsis raciborskii (Woloszynska) Seenayya and Subba Raju and Aphanizomenon issatschenkoi (Usačev) Proshkina–Lavrenko, respectively [77][78]. Therefore, many concerns have been raised related to the probability of misidentifications only relying on morphological characters under a light microscope, particularly when heterocysts and akinetes are not visible for nostocacean cyanobacteria [79][80][81][82][83][84]. In fact, although necessary, the controversy over the past decades on cyanobacterial taxonomy regarding Nostocales order, in particular, has also increased the confusion for a proper identification [64][65][66][67][69][71][73][85][86]. This can have major implications for the previous knowledge regarding the distribution and dynamics of species-specific blooms and their ecology and toxicity [87]. Therefore, polyphasic approaches are crucial for the identification and characterization of isolated cyanobacterial strains [71][88], allowing ulterior DNA sequence match and identification through phylogenetic affiliation, along with ecological and toxicological features [84][89][90]. This is the basis for a deeper exploration of global distribution patterns of cyanobacterial species by comparing strains from diverse geographical origins or from time-dispersed blooms [75][91].

2.2. Co-Dominance and Dynamics of Cyanobacterial Blooms

Cyanobacterial blooms are frequently co-dominated by several species (some of which can be very similar under a microscope and difficult to distinguish and identify correctly [79][92]). Moreover, it is known that growth requirements can vary greatly between different cyanobacterial species [19][22][52][93]. For instance, in spite of the relationship frequently reported between the occurrence of cyanobacterial blooms and eutrophication, blooms can occur under low levels of inorganic nitrogen and/or phosphorus, depending on the dominant species [22][84][94][95]. Then again, climate change conditions produce variations in the physiological responses of cyanobacterial cells and lead to important changes in the composition of bloom-dominating strains and, consequently, impact the whole dynamics and toxicity potential of a cyanobacterial bloom [30][96]. Nitrogen-fixing cyanobacteria, in particular, can take special advantage of warmer and CO2-rich conditions from climate change [96][97] and increase their geographic range of proliferation in the near future. In fact, as referred above, several Nostocales invasive diazotrophic and potentially toxic species (such as Raphidiopsis raciborskii, Cuspidothrix issatschenkoi and Sphaerospermopsis aphanizomenoides) have already been increasingly reported at higher latitudes [98][99][100][101][102][103][104]. On the other hand, during a bloom, the co-occurrence of different strains from a same species is also common, which makes it impossible to differentiate them exclusively using morphological features [79][90]. The phenotypic plasticity of some species (namely the invasive R. raciborskii and S. aphanizomenoides) can also correspond to intraspecific genetic heterogeneity even among strains from the same geographical origin [90][105], suggesting a microevolution that can provide these species an increasing expansion potential. These species-specific strains may diverse significantly in their ecological requirements and/or toxic potential [76][84][89][106][107][108], with implications not only for the bloom development and dynamics, but also for the toxicity outcomes and health risks, depending on the ratio of non-toxic vs. toxic strains. Therefore, the search for intraspecific information is becoming more and more important to understand local to global biogeographical, ecological and toxicity patterns. Here, DNA-based molecular methodologies play a crucial role not only by helping to overcome misidentifications based on morphological features but also by providing strain-specific data to track variations of cyanobacterial strains from geographically different regions [75][109][110][111] or re-incidences of blooming strains over time in the same water body [79][90][112][113].

2.3. Intraspecific Cyanotoxin Production Potential

As discussed above, the taxonomic confusion and controversy has also had an impact on the characterization of which cyanotoxins can be produced by each cyanobacterial species [64]. Additionally, each species can have toxic and non-toxic genotypes [114][115][116][117], which brings even more entropy into toxicological studies. The synthesis of different cyanotoxins relies on the presence of specific gene clusters [118][119][120], and some cyanobacteria can also have biosynthesis gene clusters for more than one cyanotoxin [11], meaning that cyanobacterial blooms can be also co-dominated by multiple-toxin-producing strains, as previously reported [121][122]. Additionally, the regulation of cyanotoxins production varies at the strain level and can be affected by environmental factors such as temperature, light, pH and concentration of nutrients such as iron and nitrogen [118] as well as the bacteria present in water [123][124]. For instance, increased water temperature can influence the toxic potential of a bloom by promoting a shift of dominance from non-toxic to toxic cyanobacterial strains; at the same time, it can also increase toxin expression in the toxic strains [115][125]. All these genetic and physiological variations at the species and strain levels have implications on the overall toxicity of a bloom and toxicity assessment for a particular species [126]. This highlights the need for more studies using polyphasic approaches at the strain level combining at least a molecular characterization along with geographical distribution, as the genotype differentiation in specific niches can be also attributed to a selection from environmental factors [114].

References

  1. Xu, H.-F.; Raanan, H.; Dai, G.-Z.; Oren, N.; Berkowicz, S.; Murik, O.; Kaplan, A.; Qiu, B.-S. Reading and Surviving the Harsh Conditions in Desert Biological Soil Crust: The Cyanobacterial Viewpoint. FEMS Microbiol. Rev. 2021, 45, fuab036.
  2. Jasser, I.; Panou, M.; Khomutovska, N.; Sandzewicz, M.; Panteris, E.; Niyatbekov, T.; Łach, Ł.; Kwiatowski, J.; Kokociński, M.; Gkelis, S. Cyanobacteria in Hot Pursuit: Characterization of Cyanobacteria Strains, Including Novel Taxa, Isolated from Geothermal Habitats from Different Ecoregions of the World. Mol. Phylogenet. Evol. 2022, 170, 107454.
  3. Perera, I.; Subashchandrabose, S.R.; Venkateswarlu, K.; Naidu, R.; Megharaj, M. Consortia of Cyanobacteria/Microalgae and Bacteria in Desert Soils: An Underexplored Microbiota. Appl. Microbiol. Biotechnol. 2018, 102, 7351–7363.
  4. Garcia-Pichel, F. Cyanobacteria. In Encyclopedia of Microbiology; Schaechter, M., Ed.; Academic Press: Cambridge, MA, USA, 2009; pp. 107–124.
  5. de Figueiredo, D.R.; Azeiteiro, U.M.; Esteves, S.M.; Gonçalves, F.J.M.; Pereira, M.J. Microcystin-Producing Blooms—A Serious Global Public Health Issue. Ecotoxicol. Environ. Saf. 2004, 59, 151–163.
  6. Wood, R. Acute Animal and Human Poisonings from Cyanotoxin Exposure—A Review of the Literature. Environ. Int. 2016, 91, 276–282.
  7. Cotterill, V.; Hamilton, D.P.; Puddick, J.; Suren, A.; Wood, S.A. Phycocyanin Sensors as an Early Warning System for Cyanobacteria Blooms Concentrations: A Case Study in the Rotorua Lakes. N. Z. J. Mar. Freshw. Res. 2019, 53, 555–570.
  8. Hilborn, E.D.; Beasley, V.R. One Health and Cyanobacteria in Freshwater Systems: Animal Illnesses and Deaths Are Sentinel Events for Human Health Risks. Toxins 2015, 7, 1374–1395.
  9. Carmichael, W.W.; Boyer, G.L. Health Impacts from Cyanobacteria Harmful Algae Blooms: Implications for the North American Great Lakes. Harmful Algae 2016, 54, 194–212.
  10. Śliwińska-Wilczewska, S.; Maculewicz, J.; Felpeto, A.B.; Latała, A. Allelopathic and Bloom-Forming Picocyanobacteria in a Changing World. Toxins 2018, 10, 48.
  11. Janssen, E.M.L. Cyanobacterial Peptides beyond Microcystins—A Review on Co-Occurrence, Toxicity, and Challenges for Risk Assessment. Water Res. 2019, 151, 488–499.
  12. Redouane, E.M.; El Amrani Zerrifi, S.; El Khalloufi, F.; Oufdou, K.; Oudra, B.; Lahrouni, M.; Campos, A.; Vasconcelos, V. Mode of Action and Fate of Microcystins in the Complex Soil-Plant Ecosystems. Chemosphere 2019, 225, 270–281.
  13. Vasconcelos, V. Cyanobacteria Toxins: Diversity and Ecological Effects. Limnetica 2001, 20, 45–58.
  14. Chorus, I.; Welker, M. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management, 2nd ed.; Chorus, I., Welker, M., Eds.; CRC Press: Boca Raton, FL, USA, 2021; ISBN 9788490225370.
  15. Cheung, M.Y.; Liang, S.; Lee, J. Toxin-Producing Cyanobacteria in Freshwater: A Review of the Problems, Impact on Drinking Water Safety, and Efforts for Protecting Public Health. J. Microbiol. 2013, 51, 1–10.
  16. Paerl, H.W.; Fulton, R.S.; Moisander, P.H.; Dyble, J. Harmful Freshwater Algal Blooms, with an Emphasis on Cyanobacteria. Sci. World J. 2001, 1, 76–113.
  17. Paerl, H.W.; Barnard, M.A. Mitigating the Global Expansion of Harmful Cyanobacterial Blooms: Moving Targets in a Human- and Climatically-Altered World. Harmful Algae 2020, 96, 101845.
  18. Huisman, J.; Codd, G.A.; Paerl, H.W.; Ibelings, B.W.; Verspagen, J.M.H.; Visser, P.M. Cyanobacterial Blooms. Nat. Rev. Microbiol. 2018, 16, 471–483.
  19. Paerl, H.W.; Otten, T.G. Duelling “CyanoHABs”: Unravelling the Environmental Drivers Controlling Dominance and Succession among Diazotrophic and Non-N2-Fixing Harmful Cyanobacteria. Environ. Microbiol. 2016, 18, 316–324.
  20. Havens, K.E.; Paerl, H.W. Climate Change at a Crossroad for Control of Harmful Algal Blooms. Environ. Sci. Technol. 2015, 49, 12605–12606.
  21. Scholz, S.N.; Esterhuizen-Londt, M.; Pflugmacher, S. Rise of Toxic Cyanobacterial Blooms in Temperate Freshwater Lakes: Causes, Correlations and Possible Countermeasures. Toxicol. Environ. Chem. 2017, 99, 543–577.
  22. O’Neil, J.M.; Davis, T.W.; Burford, M.A.; Gobler, C.J. The Rise of Harmful Cyanobacteria Blooms: The Potential Roles of Eutrophication and Climate Change. Harmful Algae 2012, 14, 313–334.
  23. Mehinto, A.C.; Smith, J.; Wenger, E.; Stanton, B.; Linville, R.; Brooks, B.W.; Sutula, M.A.; Howard, M.D.A. Synthesis of Ecotoxicological Studies on Cyanotoxins in Freshwater Habitats—Evaluating the Basis for Developing Thresholds Protective of Aquatic Life in the United States. Sci. Total Environ. 2021, 795, 148864.
  24. Weralupitiya, C.; Wanigatunge, R.P.; Gunawardana, D.; Vithanage, M.; Magana-Arachchi, D. Cyanotoxins Uptake and Accumulation in Crops: Phytotoxicity and Implications on Human Health. Toxicon 2022, 211, 21–35.
  25. Paerl, H.W.; Otten, T.G. Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls. Microb. Ecol. 2013, 65, 995–1010.
  26. Corbel, S.; Mougin, C.; Bouaïcha, N. Cyanobacterial Toxins: Modes of Actions, Fate in Aquatic and Soil Ecosystems, Phytotoxicity and Bioaccumulation in Agricultural Crops. Chemosphere 2014, 96, 1–15.
  27. Ger, K.A.; Urrutia-Cordero, P.; Frost, P.C.; Hansson, L.A.; Sarnelle, O.; Wilson, A.E.; Lürling, M. The Interaction between Cyanobacteria and Zooplankton in a More Eutrophic World. Harmful Algae 2016, 54, 128–144.
  28. Paerl, H.W.; Gardner, W.S.; Havens, K.E.; Joyner, A.R.; McCarthy, M.J.; Newell, S.E.; Qin, B.; Scott, J.T. Mitigating Cyanobacterial Harmful Algal Blooms in Aquatic Ecosystems Impacted by Climate Change and Anthropogenic Nutrients. Harmful Algae 2016, 54, 213–222.
  29. Paerl, H.W. Mitigating Toxic Planktonic Cyanobacterial Blooms in Aquatic Ecosystems Facing Increasing Anthropogenic and Climatic Pressures. Toxins 2018, 10, 76.
  30. Visser, P.M.; Verspagen, J.M.H.; Sandrini, G.; Stal, L.J.; Matthijs, H.C.P.; Davis, T.W.; Paerl, H.W.; Huisman, J. How Rising CO2 and Global Warming May Stimulate Harmful Cyanobacterial Blooms. Harmful Algae 2016, 54, 145–159.
  31. Watson, S.B.; Miller, C.; Arhonditsis, G.; Boyer, G.L.; Carmichael, W.; Charlton, M.N.; Confesor, R.; Depew, D.C.; Höök, T.O.; Ludsin, S.A.; et al. The Re-Eutrophication of Lake Erie: Harmful Algal Blooms and Hypoxia. Harmful Algae 2016, 56, 44–66.
  32. Bullerjahn, G.S.; McKay, R.M.; Davis, T.W.; Baker, D.B.; Boyer, G.L.; D’Anglada, L.V.; Doucette, G.J.; Ho, J.C.; Irwin, E.G.; Kling, C.L.; et al. Global Solutions to Regional Problems: Collecting Global Expertise to Address the Problem of Harmful Cyanobacterial Blooms. A Lake Erie Case Study. Harmful Algae 2016, 54, 223–238.
  33. Stewart, I.; Webb, P.M.; Schluter, P.J.; Shaw, G.R. Recreational and Occupational Field Exposure to Freshwater Cyanobacteria—A Review of Anecdotal and Case Reports, Epidemiological Studies and the Challenges for Epidemiologic Assessment. Environ. Health 2006, 5, 6.
  34. Carmichael, W.W. Cyanobacteria Secondary Metabolites—The Cyanotoxins. J. Appl. Bacteriol. 1992, 72, 445–459.
  35. Manning, S.R.; Nobles, D.R. Impact of Global Warming on Water Toxicity: Cyanotoxins. Curr. Opin. Food Sci. 2017, 18, 14–20.
  36. Huang, I.S.; Zimba, P.V. Cyanobacterial Bioactive Metabolites—A Review of Their Chemistry and Biology. Harmful Algae 2019, 83, 42–94.
  37. Wiegand, C.; Pflugmacher, S. Ecotoxicological Effects of Selected Cyanobacterial Secondary Metabolites a Short Review. Toxicol. Appl. Pharmacol. 2005, 203, 201–218.
  38. Smith, J.L.; Boyer, G.L.; Zimba, P. V A Review of Cyanobacterial Odorous and Bioactive Metabolites: Impacts and Management Alternatives in Aquaculture. Aquaculture 2008, 208, 5–20.
  39. Svirčev, Z.; Lalić, D.; Bojadžija Savić, G.; Tokodi, N.; Drobac Backović, D.; Chen, L.; Meriluoto, J.; Codd, G.A. Global Geographical and Historical Overview of Cyanotoxin Distribution and Cyanobacterial Poisonings; Springer: Berlin/Heidelberg, Germany, 2019; Volume 93, ISBN 0123456789.
  40. He, X.; Liu, Y.L.; Conklin, A.; Westrick, J.; Weavers, L.K.; Dionysiou, D.D.; Lenhart, J.J.; Mouser, P.J.; Szlag, D.; Walker, H.W. Toxic Cyanobacteria and Drinking Water: Impacts, Detection, and Treatment. Harmful Algae 2016, 54, 174–193.
  41. Cao, L.; Massey, I.Y.; Feng, H.; Yang, F. A Review of Cardiovascular Toxicity of Microcystins. Toxins 2019, 11, 507.
  42. Svirčev, Z.; Drobac, D.; Tokodi, N.; Mijović, B.; Codd, G.A.; Meriluoto, J. Toxicology of Microcystins with Reference to Cases of Human Intoxications and Epidemiological Investigations of Exposures to Cyanobacteria and Cyanotoxins. Arch. Toxicol. 2017, 91, 621–650.
  43. Schreidah, C.M.; Ratnayake, K.; Senarath, K.; Karunarathne, A. Microcystins: Biogenesis, Toxicity, Analysis, and Control. Chem. Res. Toxicol. 2020, 33, 2225–2246.
  44. Du, X.; Liu, H.; Yuan, L.; Wang, Y.; Ma, Y.; Wang, R.; Chen, X.; Losiewicz, M.D.; Guo, H.; Zhang, H. The Diversity of Cyanobacterial Toxins on Structural Characterization, Distribution and Identification: A Systematic Review. Toxins 2019, 11, 530.
  45. Koreiviene, J.; Anne, O.; Kasperovičiene, J.; Burškyte, V. Cyanotoxin Management and Human Health Risk Mitigation in Recreational Waters. Environ. Monit. Assess. 2014, 186, 4443–4459.
  46. Testai, E.; Scardala, S.; Vichi, S.; Buratti, F.M.; Funari, E. Risk to Human Health Associated with the Environmental Occurrence of Cyanobacterial Neurotoxic Alkaloids Anatoxins and Saxitoxins. Crit. Rev. Toxicol. 2016, 46, 385–419.
  47. O’Neill, K.; Musgrave, I.F.; Humpage, A. Low Dose Extended Exposure to Saxitoxin and Its Potential Neurodevelopmental Effects: A Review. Environ. Toxicol. Pharmacol. 2016, 48, 7–16.
  48. Moreira, C.; Azevedo, J.; Antunes, A.; Vasconcelos, V. Cylindrospermopsin: Occurrence, Methods of Detection and Toxicology. J. Appl. Microbiol. 2013, 114, 605–620.
  49. Scarlett, K.R.; Kim, S.; Lovin, L.M.; Chatterjee, S.; Scott, J.T.; Brooks, B.W. Global Scanning of Cylindrospermopsin: Critical Review and Analysis of Aquatic Occurrence, Bioaccumulation, Toxicity and Health Hazards. Sci. Total Environ. 2020, 738, 139807.
  50. Hinojosa, M.G.; Prieto, A.I.; Gutiérrez-Praena, D.; Moreno, F.J.; Cameán, A.M.; Jos, A. Neurotoxic Assessment of Microcystin-LR, Cylindrospermopsin and Their Combination on the Human Neuroblastoma SH-SY5Y Cell Line. Chemosphere 2019, 224, 751–764.
  51. Hinojosa, M.G.; Gutiérrez-Praena, D.; Prieto, A.I.; Guzmán-Guillén, R.; Jos, A.; Cameán, A.M. Neurotoxicity Induced by Microcystins and Cylindrospermopsin: A Review. Sci. Total Environ. 2019, 668, 547–565.
  52. Chorus, I.; Fastner, J.; Welker, M. Cyanobacteria and Cyanotoxins in a Changing Environment: Concepts, Controversies, Challenges. Water 2021, 13, 2463.
  53. Edwards, C.; Graham, D.; Fowler, N.; Lawton, L.A. Biodegradation of Microcystins and Nodularin in Freshwaters. Chemosphere 2008, 73, 1315–1321.
  54. Bi, X.; Dai, W.; Wang, X.; Dong, S.; Zhang, S.; Zhang, D.; Wu, M. Microcystins Distribution, Bioaccumulation, and Microcystis Genotype Succession in a Fish Culture Pond. Sci. Total Environ. 2019, 688, 380–388.
  55. Onyango, D.M.; Orina, P.S.; Ramkat, R.C.; Kowenje, C.; Githukia, C.M.; Lusweti, D.; Lung’ayia, H.B.O. Review of Current State of Knowledge of Microcystin and Its Impacts on Fish in Lake Victoria. Lakes Reserv. 2020, 25, 350–361.
  56. Vareli, K.; Zarali, E.; Zacharioudakis, G.S.A.; Vagenas, G.; Varelis, V.; Pilidis, G.; Briasoulis, E.; Sainis, I. Microcystin Producing Cyanobacterial Communities in Amvrakikos Gulf (Mediterranean Sea, NW Greece) and Toxin Accumulation in Mussels (Mytilus galloprovincialis). Harmful Algae 2012, 15, 109–118.
  57. Preece, E.P.; Hardy, F.J.; Moore, B.C.; Bryan, M. A Review of Microcystin Detections in Estuarine and Marine Waters: Environmental Implications and Human Health Risk. Harmful Algae 2017, 61, 31–45.
  58. Zhu, J.; Ren, X.; Liu, H.; Liang, C. Effect of Irrigation with Microcystins-Contaminated Water on Growth and Fruit Quality of Cucumis sativus L. and the Health Risk. Agric. Water Manag. 2018, 204, 91–99.
  59. Romero-Oliva, C.S.; Contardo-Jara, V.; Block, T.; Pflugmacher, S. Accumulation of Microcystin Congeners in Different Aquatic Plants and Crops—A Case Study from Lake Amatitlán, Guatemala. Ecotoxicol. Environ. Saf. 2014, 102, 121–128.
  60. Pham, T.L.; Utsumi, M. An Overview of the Accumulation of Microcystins in Aquatic Ecosystems. J. Environ. Manag. 2018, 213, 520–529.
  61. Weirich, C.A.; Miller, T.R. Freshwater Harmful Algal Blooms: Toxins and Children’s Health. Curr. Probl. Pediatr. Adolesc. Health Care 2014, 44, 2–24.
  62. Otten, T.G.; Paerl, H.W. Health Effects of Toxic Cyanobacteria in U.S. Drinking and Recreational Waters: Our Current Understanding and Proposed Direction. Curr. Environ. Health Rep. 2015, 2, 75–84.
  63. Palinska, K.A.; Surosz, W. Taxonomy of Cyanobacteria: A Contribution to Consensus Approach. Hydrobiologia 2014, 740, 1–11.
  64. Cirés, S.; Ballot, A. A Review of the Phylogeny, Ecology and Toxin Production of Bloom-Forming Aphanizomenon spp. and Related Species within the Nostocales (Cyanobacteria). Harmful Algae 2016, 54, 21–43.
  65. Hindák, F. Morphological Variation of Four Planktic Nostocalean Cyanophytes—Members of the Genus Aphanizomenon or Anabaena? Hydrobiologia 2000, 438, 107–116.
  66. Li, R.; Carmichael, W.W.; Liu, Y.; Watanabe, M.M. Taxonomic Re-Evaluation of Aphanizomenon flos-aquae NH-5 Based on Morphology and 16S rRNA Gene Sequences. Hydrobiologia 2000, 438, 99–105.
  67. Komárek, J.; Zapomelová, E. Planktic Morphospecies of the Cyanobacterial Genus Anabaena = Subg. Dolichospermum—2. Part: Straight Types. Fottea 2008, 8, 1–14.
  68. Zapomělová, E.; Skácelová, O.; Pumann, P.; Kopp, R.; Janeček, E. Polyphasic Characterization of Three Strains of Anabaena reniformis and Aphanizomenon aphanizomenoides (Cyanobacteria) and Their Reclassification To Sphaerospermum gen. nov. (Incl. Anabaena kisseleviana) (45:1363–73). J. Phycol. 2010, 46, 415.
  69. Zapomělová, E.; Hrouzek, P.; Řezanka, T.; Jezberová, J.; Řeháková, K.; Hisem, D.; Komárková, J. Polyphasic Characterization of Dolichospermum spp. and Sphaerospermopsis spp. (Nostocales, Cyanobacteria): Morphology, 16S rRNA Gene Sequences and Fatty Acid and Secondary Metabolite Profiles. J. Phycol. 2011, 47, 1152–1163.
  70. Gama, W.A.; Rigonato, J.; Fiore, M.F.; Sant’Anna, C.L. New Insights into Chroococcus (Cyanobacteria) and Two Related Genera: Cryptococcum gen. nov. and Inacoccus gen. nov. Eur. J. Phycol. 2019, 54, 315–325.
  71. Komárek, J. A Polyphasic Approach for the Taxonomy of Cyanobacteria: Principles and Applications. Eur. J. Phycol. 2016, 51, 346–353.
  72. Komárková, J.; Jezberová, J.; Komárek, O.; Zapomělová, E. Variability of Chroococcus (Cyanobacteria) Morphospecies with Regard to Phylogenetic Relationships. Hydrobiologia 2010, 639, 69–83.
  73. Zapomělová, E.; Jezberová, J.; Hrouzek, P.; Hisem, D.; Řeháková, K.; Komárková, J. Polyphasic Characterization of Three Strains of Anabaena reniformis and Aphanizomenon aphanizomenoides (Cyanobacteria) and Their Reclassification to Sphaerospermum gen. nov. (Incl. Anabaena kisseleviana). J. Phycol. 2009, 45, 1363–1373.
  74. Komárek, J. The Cyanobacterial Genus Macrospermum. Fottea 2008, 8, 79–86.
  75. Zapomělová, E.; Skácelová, O.; Pumann, P.; Kopp, R.; Janeček, E. Biogeographically Interesting Planktonic Nostocales (Cyanobacteria) in the Czech Republic and Their Polyphasic Evaluation Resulting in Taxonomic Revisions of Anabaena bergii Ostenfeld 1908 (Chrysosporum gen. nov.) and A. tenericaulis Nygaard 1949 (Dolichospermum tenericaule comb. nova). Hydrobiologia 2012, 698, 353–365.
  76. Zapomělová, E.; Řeháková, K.; Jezberová, J.; Komárková, J. Polyphasic Characterization of Eight Planktonic Anabaena Strains (Cyanobacteria) with Reference to the Variability of 61 Anabaena Populations Observed in the Field. Hydrobiologia 2010, 639, 99–113.
  77. Aguilera, A.; Gómez, E.B.; Kaštovský, J.; Echenique, R.O.; Salerno, G.L. The Polyphasic Analysis of Two Native Raphidiopsis Isolates Supports the Unification of the Genera Raphidiopsis and Cylindrospermopsis (Nostocales, Cyanobacteria). Phycologia 2018, 57, 130–146.
  78. Rajaniemi, P.; Komárek, J.; Willame, R.; Hrouzek, P.; Kaštovská, K.; Hoffmann, L.; Sivonen, K. Taxonomic Consequences from the Combined Molecular and Phenotype Evaluation of Selected Anabaena and Aphanizomenon Strains. Algol. Stud. Arch. Für Hydrobiol. 2005, 117, 371–391.
  79. de Figueiredo, D.R.; Lopes, A.R.; Pereira, M.J.; Polónia, A.R.; Castro, B.B.; Gonçalves, F.; Gomes, N.C.M.; Cleary, D.F.R. Bacterioplankton Community Shifts during a Spring Bloom of Aphanizomenon gracile and Sphaerospermopsis aphanizomenoides at a Temperate Shallow Lake. Hydrobiology 2022, 1, 499–517.
  80. Choi, H.J.; Joo, J.H.; Kim, J.H.; Wang, P.; Ki, J.S.; Han, M.S. Morphological Characterization and Molecular Phylogenetic Analysis of Dolichospermum hangangense (Nostocales, Cyanobacteria) sp. nov. from Han River, Korea. Algae 2018, 33, 143–156.
  81. Johansen, J.R.; Kovacik, L.; Casamatta, D.A.; Fučiková, K.; Kaštovský, J. Utility of 16S-23S ITS Sequence and Secondary Structure for Recognition of Intrageneric and Intergeneric Limits within Cyanobacterial Taxa: Leptolyngbya corticola sp. nov. (Pseudanabaenaceae, Cyanobacteria). Nova Hedwig. 2011, 92, 283–302.
  82. Moore, D.; McGregor, G.B.; Shaw, G. Morphological Changes during Akinete Germination in Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria). J. Phycol. 2004, 40, 1098–1105.
  83. Ryu, H.S.; Shin, R.Y.; Lee, J.H. Morphology and Taxonomy of the Aphanizomenon spp. (Cyanophyceae) and Related Species in the Nakdong River, South Korea. J. Ecol. Environ. 2016, 41, 6.
  84. de Figueiredo, D.R.; Gonçalves, A.M.M.; Castro, B.B.; Gonçalves, F.; Pereira, M.J.; Correia, A. Differential Inter-and Intra-Specific Responses of Aphanizomenon Strains to Nutrient Limitation and Algal Growth Inhibition. J. Plankton Res. 2011, 33, 1606–1616.
  85. Komárek, J. Modern Taxonomic Revision of Planktic Nostocacean Cyanobacteria: A Short Review of Genera. Hydrobiologia 2010, 639, 231–243.
  86. Komárek, J. Cyanobacterial Taxonomy: Current Problems and Prospects for the Integration of Traditional and Molecular Approaches. Algae 2006, 21, 349–375.
  87. Österholm, J.; Popin, R.V.; Fewer, D.P.; Sivonen, K. Phylogenomic Analysis of Secondary Metabolism in the Toxic Cyanobacterial Genera Anabaena, Dolichospermum and Aphanizomenon. Toxins 2020, 12, 248.
  88. Komárek, J. Quo Vadis, Taxonomy of Cyanobacteria (2019). Fottea 2020, 20, 104–110.
  89. Sanchis, D.; Carrasco, D.; Quesada, A. The Genus Microcystis (Microcystaceae/Cyanobacteria) from a Spanish Reservoir: A Contribution to the Definition of Morphological Variations. Nova Hedwig. 2004, 79, 479–495.
  90. de Figueiredo, D.R.; Alves, A.; Pereira, M.J.; Correia, A. Molecular Characterization of Bloom-Forming Aphanizomenon Strains Isolated from Vela Lake (Western Central Portugal). J. Plankton Res. 2010, 32, 239–252.
  91. Werner, V.R.; Laughinghouse, H.D., IV; Fiore, M.F.; Sant’anna, C.L.; Hoff, C.; de Souza Santos, K.R.; Neuhaus, E.B.; Molica, R.J.R.; Honda, R.Y.; Echenique, R.O.; et al. Morphological and Molecular Studies of Sphaerospermopsis torques-reginae (Cyanobacteria, Nostocales) from South American Water Blooms. Phycologia 2012, 51, 228–238.
  92. Lv, X.; Cheng, Y.; Zhang, S.; Hu, Z.; Xiao, P.; Zhang, H.; Geng, R.; Li, R. Polyphasic Characterization and Taxonomic Evaluation of a Bloom-Forming Strain Morphologically Resembling Radiocystis fernandoi (Chroococcales, Cyanobacteria) from Lake Erhai, China. Diversity 2022, 14, 816.
  93. Tanvir, R.U.; Hu, Z.; Zhang, Y.; Lu, J. Cyanobacterial Community Succession and Associated Cyanotoxin Production in Hypereutrophic and Eutrophic Freshwaters. Environ. Pollut. 2021, 290, 118056.
  94. de Figueiredo, D.R.; Reboleira, A.S.S.P.; Antunes, S.C.; Abrantes, N.; Azeiteiro, U.; Gonçalves, F.; Pereira, M.J.; Gonçalves, F.; Figueiredo, D.R. The Effect of Environmental Parameters and Cyanobacterial Blooms on Phytoplankton Dynamics of a Portuguese Temperate Lake. Hydrobiologia 2006, 568, 145–157.
  95. Gobler, C.J.; Burkholder, J.A.M.; Davis, T.W.; Harke, M.J.; Johengen, T.; Stow, C.A.; Van de Waal, D.B. The Dual Role of Nitrogen Supply in Controlling the Growth and Toxicity of Cyanobacterial Blooms. Harmful Algae 2016, 54, 87–97.
  96. Ma, J.; Wang, P. Effects of Rising Atmospheric CO2 Levels on Physiological Response of Cyanobacteria and Cyanobacterial Bloom Development: A Review. Sci. Total Environ. 2021, 754, 141889.
  97. Symes, E.; van Ogtrop, F.F. The Effect of Pre-Industrial and Predicted Atmospheric CO2 Concentrations on the Development of Diazotrophic and Non-Diazotrophic Cyanobacterium: Dolichospermum circinale and Microcystis aeruginosa. Harmful Algae 2019, 88, 101536.
  98. Rzymski, P.; Brygider, A.; Kokociński, M. On the Occurrence and Toxicity of Cylindrospermopsis raciborskii in Poland. Limnol. Rev. 2017, 17, 23–29.
  99. Fastner, J.; Rücker, J.; Stüken, A.; Preußel, K.; Nixdorf, B.; Chorus, I.; Köhler, A.; Wiedner, C. Occurrence of the Cyanobacterial Toxin Cylindrospermopsin in Northeast Germany. Environ. Toxicol. 2007, 22, 26–32.
  100. Stüken, A.; Rücker, J.; Endrulat, T.; Preussel, K.; Hemm, M.; Nixdorf, B.; Karsten, U.; Wiedner, C. Distribution of Three Alien Cyanobacterial Species (Nostocales) in Northeast Germany: Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 2006, 45, 696–703.
  101. Kim, Y.-J.; Park, H.-K.; Kim, I.-S. Invasion and Toxin Production by Exotic Nostocalean cyanobacteria (Cuspidothrix, Cylindrospermopsis, and Sphaerospermopsis) in the Nakdong River, Korea. Harmful Algae 2020, 100, 101954.
  102. Budzyńska, A.; Gołdyn, R. Domination of Invasive Nostocales (Cyanoprokaryota) at 52°N Latitude. Phycol. Res. 2017, 65, 322–332.
  103. Budzyńska, A.; Rosińska, J.; Pełechata, A.; Toporowska, M.; Napiórkowska-Krzebietke, A.; Kozak, A.; Messyasz, B.; Pęczuła, W.; Kokociński, M.; Szeląg-Wasielewska, E.; et al. Environmental Factors Driving the Occurrence of the Invasive Cyanobacterium Sphaerospermopsis aphanizomenoides (Nostocales) in Temperate Lakes. Sci. Total Environ. 2019, 650, 1338–1347.
  104. Kokociński, M.; Soininen, J. New Insights into the Distribution of Alien Cyanobacterium Chrysosporum bergii (Nostocales, Cyanobacteria). Phycol. Res. 2019, 67, 208–214.
  105. Zheng, L.; Liu, Y.; Li, R.; Yang, Y.; Jiang, Y. Recent Advances in the Ecology of Bloom-Forming Raphidiopsis (Cylindrospermopsis) raciborskii: Expansion in China, Intraspecific Heterogeneity and Critical Factors for Invasion. Int. J. Environ. Res. Public Health 2023, 20, 1984.
  106. Galvanese, E.F.; Padial, A.A.; Aubriot, L. Acclimation at High Temperatures Increases the Ability of Raphidiopsis raciborskii (Cyanobacteria) to Withstand Phosphate Deficiency and Reveals Distinct Strain Responses. Eur. J. Phycol. 2019, 54, 359–368.
  107. Joung, S.-H.; Oh, H.-M.; Ko, S.-R.; Ahn, C.-Y. Correlations between Environmental Factors and Toxic and Non-Toxic Microcystis Dynamics during Bloom in Daechung Reservoir, Korea. Harmful Algae 2011, 10, 188–193.
  108. Yoshida, M.; Yoshida, T.; Satomi, M.; Takashima, Y.; Hosoda, N.; Hiroishi, S. Intra-Specific Phenotypic and Genotypic Variation in Toxic Cyanobacterial Microcystis Strains. J. Appl. Microbiol. 2008, 105, 407–415.
  109. Moreira, C.; Fathalli, A.; Vasconcelos, V.; Antunes, A. Genetic Diversity and Structure of the Invasive Toxic Cyanobacterium Cylindrospermopsis raciborskii. Curr. Microbiol. 2011, 62, 1590–1595.
  110. Haande, S.; Rohrlack, T.; Ballot, A.; Røberg, K.; Skulberg, R.; Beck, M.; Wiedner, C. Genetic Characterisation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) Isolates from Africa and Europe. Harmful Algae 2008, 7, 692–701.
  111. Gugger, M.; Molica, R.; Le Berre, B.; Dufour, P.; Bernard, C.; Humbert, J.-F. Genetic Diversity of Cylindrospermopsis Strains (Cyanobacteria) Isolated from Four Continents. Appl. Environ. Microbiol. 2005, 71, 1097–1100.
  112. Hur, M.; Lee, I.; Tak, B.-M.; Lee, H.J.; Yu, J.J.; Cheon, S.U.; Kim, B.-S. Temporal Shifts in Cyanobacterial Communities at Different Sites on the Nakdong River in Korea. Water Res. 2013, 47, 6973–6982.
  113. Wilhelm, S.W.; Farnsley, S.E.; LeCleir, G.R.; Layton, A.C.; Satchwell, M.F.; DeBruyn, J.M.; Boyer, G.L.; Zhu, G.; Paerl, H.W. The Relationships between Nutrients, Cyanobacterial Toxins and the Microbial Community in Taihu (Lake Tai), China. Harmful Algae 2011, 10, 207–215.
  114. Capelli, C.; Ballot, A.; Cerasino, L.; Papini, A.; Salmaso, N. Biogeography of Bloom-Forming Microcystin Producing and Non-Toxigenic Populations of Dolichospermum lemmermannii (Cyanobacteria). Harmful Algae 2017, 67, 1–12.
  115. Davis, T.W.; Berry, D.L.; Boyer, G.L.; Gobler, C.J. The Effects of Temperature and Nutrients on the Growth and Dynamics of Toxic and Non-Toxic Strains of Microcystis during Cyanobacteria Blooms. Harmful Algae 2009, 8, 715–725.
  116. Kurmayer, R.; Christiansen, G.; Fastner, J.; Börner, T. Abundance of Active and Inactive Microcystin Genotypes in Populations of the Toxic Cyanobacterium Planktothrix spp. Environ. Microbiol. 2004, 6, 831–841.
  117. Johansson, E.; Legrand, C.; Björnerås, C.; Godhe, A.; Mazur-Marzec, H.; Säll, T.; Rengefors, K. High Diversity of Microcystin Chemotypes within a Summer Bloom of the Cyanobacterium Microcystis botrys. Toxins 2019, 11, 698.
  118. Pearson, L.A.; Dittmann, E.; Mazmouz, R.; Ongley, S.E.; D’Agostino, P.M.; Neilan, B.A. The Genetics, Biosynthesis and Regulation of Toxic Specialized Metabolites of Cyanobacteria. Harmful Algae 2016, 54, 98–111.
  119. Rantala-Ylinen, A.; Känä, S.; Wang, H.; Rouhiainen, L.; Wahlsten, M.; Rizzi, E.; Berg, K.; Gugger, M.; Sivonen, K. Anatoxin-a Synthetase Gene Cluster of the Cyanobacterium Anabaena sp. strain 37 and Molecular Methods to Detect Potential Producers. Appl. Environ. Microbiol. 2011, 77, 7271–7278.
  120. Méjean, A.; Paci, G.; Gautier, V.; Ploux, O. Biosynthesis of Anatoxin-a and Analogues (Anatoxins) in Cyanobacteria. Toxicon 2014, 91, 15–22.
  121. Burford, M.A.; Davis, T.W.; Orr, P.T.; Sinha, R.; Willis, A.; Neilan, B. Nutrient-Related Changes in the Toxicity of Field Blooms of the Cyanobacterium, Cylindrospermopsis raciborskii. FEMS Microbiol. Ecol. 2014, 89, 135–148.
  122. Lei, L.; Lei, M.; Cheng, N.; Chen, Z.; Xiao, L.; Han, B.P.; Lin, Q. Nutrient Regulation of Relative Dominance of Cylindrospermopsin-Producing and Non-Cylindrospermopsin-Producing Raphidiopsis raciborskii. Front. Microbiol. 2021, 12, 793544.
  123. Shimizu, K.; Maseda, H.; Okano, K.; Itayama, T.; Kawauchi, Y.; Chen, R.; Utsumi, M.; Zhang, Z.; Sugiura, N. How Microcystin-Degrading Bacteria Express Microcystin Degradation Activity. Lakes Reserv. 2011, 16, 169–178.
  124. Kormas, K.A.; Lymperopoulou, D.S. Cyanobacterial Toxin Degrading Bacteria: Who Are They? Biomed. Res. Int. 2013, 2013, 1463894.
  125. Dziallas, C.; Grossart, H.P. Increasing Oxygen Radicals and Water Temperature Select for Toxic Microcystis sp. PLoS ONE 2011, 6, e25569.
  126. Omidi, A.; Esterhuizen-Londt, M.; Pflugmacher, S. Still Challenging: The Ecological Function of the Cyanobacterial Toxin Microcystin–What We Know so Far. Toxin Rev. 2018, 37, 87–105.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
Upload a video for this entry
Information
Subjects: Marine & Freshwater Biology
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Daniela R. de Figueiredo
View Times: 80
Revisions: 2 times (View History)
Update Date: 18 Jan 2024
Table of Contents
    1000/1000
    Hot Most Recent
    Video Production Service
    Feedback