African Journal of
Environmental Science and Technology

  • Abbreviation: Afr. J. Environ. Sci. Technol.
  • Language: English
  • ISSN: 1996-0786
  • DOI: 10.5897/AJEST
  • Start Year: 2007
  • Published Articles: 1126

Full Length Research Paper

Characterization of cyanobacteria microcystins (cyanotoxins) blooming in the Dams of Northern Morocco

Mustapha Ouhsassi
  • Mustapha Ouhsassi
  • Laboratory of Biology and Health, Biotechnology and Applied Microbiology, Faculty of Sciences, Abdelmalek Essaadi University, Tétouan, Morocco.
  • Google Scholar
El Ouardy Khay
  • El Ouardy Khay
  • Laboratory of Biology and Health, Biotechnology and Applied Microbiology, Faculty of Sciences, Abdelmalek Essaadi University, Tétouan, Morocco.
  • Google Scholar
Anass El Laghdach
  • Anass El Laghdach
  • Laboratory of Water, Environmental Studies and Analysis, Department of Chemistry, Faculty of Sciences, Abdelmalek Essaâdi University, Tétouan, Morocco.
  • Google Scholar
Farid Ben Abdelouahab
  • Farid Ben Abdelouahab
  • Laboratory Materials and Radiation, Department of Physique, Faculty of Science, Tétouan, Faculty of Science, Abdelmalek Essaâdi University, BP 2121, Tétouan 93002, Morocco.
  • Google Scholar
Abdeltif El Ouahrani
  • Abdeltif El Ouahrani
  • Laboratory of Biology and Health, Biotechnology and Applied Microbiology, Faculty of Sciences, Abdelmalek Essaadi University, Tétouan, Morocco.
  • Google Scholar
Mohamed Idaomar
  • Mohamed Idaomar
  • Laboratory of Biology and Health, Biotechnology and Applied Microbiology, Faculty of Sciences, Abdelmalek Essaadi University, Tétouan, Morocco.
  • Google Scholar
Jamal Abrini
  • Jamal Abrini
  • Laboratory of Biology and Health, Biotechnology and Applied Microbiology, Faculty of Sciences, Abdelmalek Essaadi University, Tétouan, Morocco.
  • Google Scholar


  •  Received: 10 December 2020
  •  Accepted: 17 February 2021
  •  Published: 31 March 2021

References

ADH (2006). Les grands barrages au Maroc. Publication de l'administration de l'hydraulique, Rabat, Maroc 123 p.

 

Ai Y, Lee S, Lee J (2020). Drinking water treatment residuals from cyanobacteria bloom-affected areas: Investigation of potential impact on agricultural land application. Science of the Total Environment 706:1-11.
Crossref

 
 

Bourrelly P (1985). Les algues d'eau douce: Initiation à la systématique. Tome III: Les algues bleues et rouges. Les Eugléniens, Péridiniens et Cryptomonadines. Société Nouvelle des Editions Bouée.

 
 

Bruno MP, Gucci PMB, Pierdominici E, Sestili P, Ioppolo A, Sechi N, Volterra L (1992). Microcystin-like toxins in different freshwater species of Oscillatoria. Toxicon 30(10):1307-1311.
Crossref

 
 

Carmichael WW (1992a). Cyanobacteria secondary metabolites the cyanotoxins. Journal of Applied Bacteriology 72(6):445-459.
Crossref

 
 

Carmichael WW (1995). Toxic Microcystis and the environment. Toxic microcystis pp.1-11.

 
 

Carmichael WW, Azevedo SM, An JS, Jochimsen EM, Lau S, Eaglesham GK (2001). Human fatalities from cyanobacteria: chemical and biological evidence for cyanotoxins. Environmental Health Perspectives 109(7):663-668.
Crossref

 
 

Cherifi O, Loudiki M (2002).Variations de la structure du lac-réservoir oligotrophe Bin El Ouidane (Maroc). Revue des Sciences de l'Eau 15(1):193-208.
Crossref

 
 

Chorus I, Bartram J, Editors (1999). Toxic Cyanobacteria in Water-A Guide to Their Public Health Consequences, Monitoring, and Management, E & FN Spon, published on behalf of the World Health Organization, New York.
Crossref

 
 

Christophoridis C, Zervou SK, Manolidi K, Katsiapi M, Moustaka-Gouni M, Kaloudis T, Hiskia A (2018). Occurrence and diversity of cyanotoxins in Greek lakes. Scientific Reports 8(1):1-22.
Crossref

 
 

Codd GA (2000). Cyanobacterial toxins, the perception of water quality, and the prioritisation of eutrophication control. Ecological Engineering 16(1):51-60.
Crossref

 
 

Diehnelt CW, Dugan NR, Peterman SM, Budde WL (2006). Identification of Microcystin Toxins from a Strain of Microcystis aeruginosa by Liquid Chromatography Introduction into a Hybrid Linear Ion Trap-Fourier Transform Ion Cyclotron Resonance Mass Spectrometer. Analytical Chemistry 78(2): 501-512.
Crossref

 
 

Diehnelt CW, Peterman SM, Budde WL (2005). Liquid chromatography-tandem mass spectrometry and accurate m/z measurements of cyclic peptide cyanobacteria toxins. Trends in Analytical Chemistry 24(7):622-634.
Crossref

 
 

Dittmann E, Börner T (2005). Genetic contributions to the risk assessment of microcystin in the environment. Toxicology and Applied Pharmacology 203(3):192-200.
Crossref

 
 

Dittmann E, Neilan BA, Erhard M, Von Döhren H, Börner T (1997). Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Molecular microbiology 26(4):779-787.
Crossref

 
 

Douma M, Ouahid Y, del Campo FF, Loudiki M, Mouhri Kh, Oudra B (2010). Identification and quantification of cyanobacterial toxins (microcystins) in two Moroccan drinking-water reservoirs (Mansour Eddahbi, Almassira). Environmental Monitoring and Assessment 160(1-4):439-450.
Crossref

 
 

El Ghachtoul Y, Alaoui Mhamidi M, Gabi H (2005). Eutrophisation des eaux des retenues des barrages Smir et Sehla (maroc): causes, conséquences et consignes de gestion. Revue des Sciences de l'Eau 18:75-89.
Crossref

 
 

Ferris JM, Hirsch CF (1991). Method for isolation and purification of Cyanobacteria. Applied and Environmental Microbiology 57(5):1448-1452.
Crossref

 
 

Filatova D, Picardo M, Núñez O, Farré M (2020). Analysis, levels and seasonal variation of cyanotoxins in freshwater ecosystems. Trends in Environmental Analytical Chemistry 26:e00091.
Crossref

 
 

Gophen M (2021). Climate Change-Enhanced Cyanobacteria Domination in Lake Kinneret: A Retrospective Overview. Water 13(2):163.
Crossref

 
 

Hayakawa K, Tsujimura S, Napolitano GE, Nakano SI, Kumagai M, Nakajima T, Jiao C (2002). Fatty acid composition as an indicator of physiological condition of the cyanobacterium miicrocystis aeruginosa. Limnology 3(1):29-35.
Crossref

 
 

Hirooka T, Akiyama Y, Tsuji N, Nakamura T, Nagase H, Hirata K, Miyamoto K (2003). Removal of hazardous phenols by microalgae under photoautotrophic conditions. Journal of Bioscience and Bioengineering 95(2):200-203.
Crossref

 
 

Hotto AM, Satchwell MF, Boyer GL (2007). Molecular characterization of potential microcystin-producing cyanobacteria in Lake Ontario embayments and nearshore waters. Applied and Environmental Microbiology 73(14):4570-8.
Crossref

 
 

Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JM, Visser PM (2018). Cyanobacterial blooms. Nature Reviews Microbiology 16(8):471-83.
Crossref

 
 

IPCC (2007). Climate change 2007: the physical sciences basis. Contribution of the Working Group I to the Fourth Assessment report of The IPCC [Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averty KB, Tignor M, Miller HL (eds). Cambridge University Press, Cambridge, United Kingdom and New York, USA.

 
 

Issaka S, Ashraf MA, (2017). Impact of soil erosion and degradation on water quality: a review. Geology, Ecology and Landscapes 1(1):1-11.
Crossref

 
 

Jacoby JM, Kann J (2007). The occurrence and response to toxic cyanobacteria in the Pacific Northwest, North America. Lake and Reservoir Management 23(2):123-143.
Crossref

 
 

Kadiri MO, Isagba S, Ogbebor JU, Omoruyi OA, Unusiotame-Owolagba TE, Lorenzi AS, Chia MA (2020). The presence of microcystins in the coastal waters of Nigeria, from the Bights of Bonny and Benin, Gulf of Guinea. Environmental Science and Pollution Research 27(28):35284-35293.
Crossref

 
 

Kenyon CN, Stanier RY (1970). Possible evolutionary significance of Polyunsaturated fatty acids in blue-green algae. Nature 227(5263):1164-1166.
Crossref

 
 

Komárek J (2016). Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia 764 (1):259-270.
Crossref

 
 

Komárek J, Anagnostidis K (2005). Cyanoprokaryota, freshwater flora of Central Europe, Gustav Fischer, Jena Stuttgart Lübeck Ulm 548 p.

 
 

Kotai J (1972). Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research, Oslo 11(69):5.

 
 

Lawton LA, Edwards C, Codd, GA (1994). Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119(7):1525-1530.
Crossref

 
 

Lindholm T, Eriksson JE, Meriluoto JAO (1989). Toxic cyanobacteria and water quality problems: Examples from a eutrophic lake on Aland, South west Finland. Water Research 23(4):481-486.
Crossref

 
 

Los DA, Mironov KS (2015). Modes of fatty acid desaturation in cyanobacteria: an update. Life 5(1):554-567.
Crossref

 
 

Loudiki M (1990). Etude limnologique d'un hydrosystème récemment aménagé dans la région de Marrakech (Maroc): apports du bassin versant, hydrochimie, algues et macrophytes (Doctoral dissertation, Aix-Marseille 3) 353 p.

 
 

Loudiki M, Bouterfas R, Mouhri K (1994). Dynamique et évaluation des apports du bassin versant et de l'état trophique du lac-réservoir Hassan I (Maroc). Revue. Faculté. Sciences. Marrakech 8:45-57.

 
 

Loudiki M, Oudra B, Sabourd B, Sbiyyaa B, Vasconcelos V, Franca S (2002). Taxonomy and geographic distribution of potentiel toxic cyanobacterial strains in Morocco. Annales de Limnologie 38(2):101-108.
Crossref

 
 

Lund HC, Lund JWG (1995). Freshwater algae: their microscopic world explored. Hong Kong: Dah Hua Ltd. ISBN 0-948737-25-5.

 
 

Mahapatra DM, Ramachandra TV (2013). Algal biofuel: bountiful lipid from Chlorococcum sp. proliferating in municipal wastewater. Current Science 105:47-55.

 
 

Major Y, Kifle D, Spoof L, Meriluoto J (2018). Cyanobacteria and microcystins in Koka reservoir (Ethiopia). Environmental Science and Pollution Research 25(27): 26861-26873.
Crossref

 
 

Malki M (1994). Etude de la communauté phytoplanctonique et des caractéristiques physico-chimiques des eaux du lac reservoir Al Massira. Thèse de Doctorat d'état, Université Hassan II, Casablanca 287p.

 
 

Miles CO, Sandvik M, Nonga HE, Rundberget T, Wilkins AL, Rise F, Ballot A (2013). Identification of microcystins in a Lake Victoria cyanobacterial bloom using LC-MS with thiol derivatization. Toxicon 70:21-31.
Crossref

 
 

Moreira C, Gomes C, Vasconcelos V, Antunes A (2020). Cyanotoxins occurrence in Portugal: A new report on their recent multiplication. Toxins 12(3):154.
Crossref

 
 

Murata N, Wada H, Gombos Z (1992). Modes of fatty-acid desaturation in cyanobacteria. Plant Cell Physiology 33:933-941.

 
 

Nagase H, Inthorn D, Oda A, Nishimura J, Kajiwara Y, Park MO, Miyamoto k (2005). Improvement of selective removal of heavy metals in cyanobacteria by NaOH treatment. Journal of Bioscience and Bioengineering 99:372-377.
Crossref

 
 

Namikoshi M, Rinehart KL, Sakai R, Stotts RR, Dahlem AM, Beasley VR, Carmichael WW, Evans WR (1992). Identification of 12 hepatotoxins from a Homer Lake bloom of the cyanobacteria Microcystis aeruginosa, Microcystis viridis, and Microcystis wesenbergii: nine new microcystins. The Journal of organic chemistry 57(3):866-872.
Crossref

 
 

Namikoshi M, Sun F, Choi BW, Rinehart KL, Carmichael WW, Evans WR, Beasley VR (1995). Seven more microcystins from homer lake cells: Application of the general method for structure assignment of peptides containing. Alpha. Beta-dehydroamino acid unit (s). The Journal of Organic Chemistry 60(12):3671-3679.
Crossref

 
 

Oudra B, Loudiki M, Sabour B, Sbiyyaa B, Vasconcelos V (2001b). Étude des blooms toxiques à cyanobactéries dans trois lacs réservoirs du Maroc: Résultats préliminaires. Revue des sciences de l'eau 15:301-313.
Crossref

 
 

Oudra B, Loudiki M, Sbiyyaa B, Martins R, Vasconcelos V, Namikoshi N (2001a). Isolation, characterisation and quantification of microcystins (heptapeptides hepatotoxins) in Microcystis aeruginosa dominated bloom of Lalla Takerkoust lake-reservoir (Morocco). Toxicon 39:1375-1381.
Crossref

 
 

Oudra B, Loudiki M, Sbiyyaa B, Vasconcelos V, Zerrouk H, El-Andaloussi-Dadi M, Darley J (1998). Occurrence of hepatotoxic Microcystis aeruginosa blooms in eutrophic Moroccan lake-reservoir. Harmful Algae, Xunta de Galicia and Intergovernamental Oceanographic Comisión (IOC) of UNESCO pp. 29-31.

 
 

Oudra B, Loudiki M, Vasconcelos V, Sabour B, Sbiyyaa B, Oufdou K, Mezrioul N (2002a). Detection and quantification of microcystins from cyanobacteria strains isolated from reservoirs and ponds in Morocco. Environmental Toxicology 17(1):32-39.
Crossref

 
 

Ouhamdouch S, Bahir M, Ouazar D, Carreira P M, Zouari K (2019). Evaluation of climate change impact on groundwater from semi-arid environment (Essaouira Basin, Morocco) using integrated approaches. Environmental Earth Sciences 78(15):449.
Crossref

 
 

Ouhsassi M, Khay EL, Bouyahya A, Abrini J (2017). Isolation and characterization of cyanobacteria strains based on the compositional approach of fatty acids: case of drinking water reservoirs in the region of Tetouan (Northern Morocco). Journal of Algal Biomass Utilization 9(1):57-67.

 
 

Passaquet C, Zabulon G, Lemoine Y, Dubacq JP, Thomas JC (1989). Lipides et pigments des fractions sub-membranaires obtenues par traitement à la digitonine chez la cyanobactérie Pseudanabaena sp. Souche M2. Bulletin de La Société Botanique de France. Actualités Botaniques 136(1):169-173.
Crossref

 
 

Paerl HW (2016). Impacts of climate change on cyanobacteria in aquatic environments. Climate change and microbial ecology: Current research and future trends pp. 5-22.
Crossref

 
 

Perrin JL, Raïs N, Chahinian N, Moulin P, Ijjaali M (2014). Water quality assessment of highly polluted rivers in a semi-arid Mediterranean zone Oued Fez and Sebou River (Morocco). Journal of Hydrology 14(510):26-34.
Crossref

 
 

Plaas HE, Paerl HW (2021). Toxic cyanobacteria: a growing threat to water and air quality. Environmental Science and Technology 55(1):44-64.
Crossref

 
 

Poon GK, Griggs LJ, Edwards C, Beattie KA, Codd GA (1993). Liquid chromatography-electrospray ionization-mass spectrometry of cyanobacterial toxins. Journal of Chromatography A 628(2):215-233.
Crossref

 
 

Quesada A, Sanchis D, Carrasco D (2004).Cyanobacteria in Spanish reservoirs. How frequently are they toxic?

View

 
 

Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111(1):1-61.
Crossref

 
 

Rouhiainen L, Sivonen K, Buikema WJ, Haselkorn R (1995). Characterization of toxin-producing cyanobacteria by using an oligonucleotide probe containing a tandemly repeated heptamer. Journal of Bacteriology 177(20):6021-6026.
Crossref

 
 

Rose E, Sabir M, Laouina A (2010). Gestion durable des eaux et des sols au Maroc: valorisation des techniques traditionnelles méditerranéennes. IRD Editions Marseille. 
Crossref

 
 

Sabour B (2002). Etude des blooms d'algues toxiques à Cyanobactéries et Haptophycées dans le lac de barrage Oued Mellah (Maroc): ecologie, écophysiologie et toxicologie. PhD thesis, Mohamedia, Morocco.

 
 

Saoudi A (2008). Isolement, culture et evaluation de la toxicite des afflorescences à microcystis sp; du barrage mexa (el-tarf) (doctoral dissertation, université de annaba-badji mokhtar).

 
 

Saoudi A, Brient L, Boucetta S, Ouzrout R, Bormans M, Bensouilah M (2017). Management of toxic cyanobacteria for drinking water production of Ain Zada Dam. Environmental Monitoring and Assessment 189(7):1-11.
Crossref

 
 

Sarsekeyeva FK, Usserbaeva AA, Zayadan BK, Mironov KS, Sidorov RA, Kozlova AY, Los DA (2014). Isolation and characterization of a new cyanobacterial strain with a unique fatty acid composition. Advances in Microbiology 4(15):1033.
Crossref

 
 

Sas H (1989). Lake restoration by reduction of nutrient loading: expectations, experiences, extrapolations. Academia Verlag Richarz, St. Augustin, Germany.

 
 

Sbiyyaa B (1997). Déterminisme, écophysiologie, toxicité et implications écologiques du bloom toxique à Microcystis aeruginosa Kütz. (Cyanobactérie) dans le lac de barrage Lalla Takerkoust (Maroc). Thèse. University. Cadi Ayyad, Marrakech 219 p.

 
 

Sharathchandra K, Rajashekhar M (2011). Total lipid and fatty acid composition in some freshwater cyanobacteria. Journal of Algal Biomass Utilization 2(2):83-97.

 
 

Shimizu K, Sano T, Kubota R, Kobayashi N, Tahara M, Obama T, Sugimoto N, Nishimura T, Ikarashi Y (2014). Effects of the Amino Acid Constituents of Microcystin Variants on Cytotoxicity to Primary Cultured Rat Hepatocytes Toxins 6:168-179.
Crossref

 
 

Thajuddin N, Subramanian G (2005). Cyanobacterial biodiversity and potential applications in biotechnology. Current Science 89(1):47-57.

 
 

Vasconcelos VM, Sivonen K, Evans WR, Carmichael WW, Namikoshi M (1996). Hepatotoxic microcystin diversity in cyanobacterial blooms collected in Portuguese freshwaters. Water Research 30(10):2377-84.
Crossref

 
 

Wiegand C, Pflugmacher S (2005). Ecotoxicological effects of selected cyanobacterial secondary metabolites a short review. Toxicology and applied pharmacology 203(3):201-218.
Crossref

 
 

Yoon JH, Shin JH, Kim MS, Sim SJ, Park TH (2006). Evaluation of conversion efficiency of light to hydrogen energy by Anabaena variabilis. International Journal of Hydrogen Energy 31:721-727.
Crossref

 
 

Yu SZ (1995). Primary prevention of hepatocellular carcinoma. Journal of gastroenterology and Hepatology 10(6):674-682.
Crossref

 
 

Zastepa A, Watson SB, Kling H, Kotak B (2017). Spatial and temporal patterns in microcystin toxins in Lake of the Woods surface waters. Lake and Reservoir Management 33(4):433-443.
Crossref