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Potential control of toxic cyanobacteria blooms with Moroccan seaweed extracts

  • Soukaina El Amrani Zerrifi
  • Zakaria Tazart
  • Fatima El Khalloufi
  • Brahim Oudra
  • Alexandre Campos
  • Vitor VasconcelosEmail author
Research Article
  • 46 Downloads

Abstract

Marine macroalgae are a promising source of diverse bioactive compounds with applications in the biocontrol of harmful cyanobacteria blooms (cyanoHABs). In this work, we evaluated the potential algicidal activities of 14 species of seaweed collected from the coast of Souiria Laqdima, Morocco. Methanol extracts were screened in solid and liquid medium against the growth of the toxic cyanobacteria Microcystis aeruginosa and the microalgae Chlorella sp. used as food supplement. The results in solid medium revealed that the algicidal activity was limited to M. aeruginosa with the extract of Bornetia secundiflora showing the highest growth inhibition activity against Microcystis (27.33 ± 0.33 mm), whereas the extracts of Laminaria digitata, Halopytis incurvus, Ulva lactuca, and Sargasum muticum showed no inhibition. In liquid medium, the results indicated that all methanolic extracts of different macroalgae tested have a significant inhibitory effect on M. aeruginosa compared with that of the negative control. The maximum inhibition rates of M. aeruginosa were produced by the extracts of Bifurcaria tuberculata, Codium elongatum, and B. secundiflora. Moreover, the extracts of B. secundiflora recorded the maximum inhibition rate of Chlorella sp. Overall, the results highlight the potential of the extracts from macroalgae to control toxic cyanobacteria species.

Keywords

CyanoHABs Microcystis Algicidal activity Seaweeds extracts Biocide effect Biocontrol 

Notes

Funding information

We acknowledge the projects TOXICROP (823860) funded by the H2020 program MSCA-RISE-2018 and the project VALORMAR (24517) of the 10/SI/2016-I&DT Empresarial-Programas Mobilizadores funded by the European Regional Development Fund (ERDF) and by the European Social Fund (ESF),

References

  1. Abdel-Latif HHA-L, Shams El-Din NG, Ibrahim HAH (2018) Antimicrobial activity of the newly recorded red alga Grateloupia doryphora collected from the Eastern Harbor, Alexandria, Egypt. J Appl Microbiol 125:1321–1332.  https://doi.org/10.1111/jam.14050 CrossRefGoogle Scholar
  2. Al-Enazi NM, Awaad AS, Zain ME, Alqasoumi SI (2017) Antimicrobial, antioxidant and anticancer activities of Laurencia catarinensis, Laurencia majuscula and Padina pavonica extracts. Saudi Pharm J 26:44–52.  https://doi.org/10.1016/j.jsps.2017.11.001 CrossRefGoogle Scholar
  3. An Z, Wang Z, Li F, Tian Z, Hu H (2008) Allelopathic inhibition on red tide microalgae Skeletonema costatum by five macroalgal extracts. Front Environ Sci Eng China 2:297–305.  https://doi.org/10.1007/s11783-008-0055-3 CrossRefGoogle Scholar
  4. Begum S, Nyandoro S, Buriyo A et al (2018) Bioactivities of extracts, debromolaurinterol and fucosterol from macroalgae species. Tanzania J Sci 44:104–116Google Scholar
  5. Catherine Q, Susanna W, Isidora ES, Mark H, Aurélie V, Jean-François H (2013) A review of current knowledge on toxic benthic freshwater cyanobacteria—ecology, toxin production and risk management. Water Res 47:5464–5479.  https://doi.org/10.1016/j.watres.2013.06.042 CrossRefGoogle Scholar
  6. Chiang I-Z, Huang W-Y, Wu J-T (2004) Allelochemicals of Botryococcus braunii (Chlorophyceae). J Phycol 40:474–480.  https://doi.org/10.1111/j.1529-8817.2004.03096.x CrossRefGoogle Scholar
  7. Demeke A (2016) Cyanobacteria blooms and biological control. Methods 3:32–38Google Scholar
  8. Gao L, Xie L (2011) Analysis of the influence of meteorological condition on cyanobacterial bloom and treatment methods in Taihu Lake. China Resour 29:35–38Google Scholar
  9. Jeong JH, Jin HJ, Sohn CH, Suh KH, Hong YK (2000) Algicidal activity of the seaweed Corallina pilulifera against red tide microalgae. J Appl Phycol 12:37–43.  https://doi.org/10.1023/A:1008139129057 CrossRefGoogle Scholar
  10. Kamaya Y, Kurogi Y, Suzuki K (2003) Acute toxicity of fatty acids to the freshwater green alga Selenastrum capricornutum. Environ Toxicol 18:289–294.  https://doi.org/10.1002/tox.10127 CrossRefGoogle Scholar
  11. Kazir M, Abuhassira Y, Robin A, Nahor O, Luo J, Israel A, Golberg A, Livney YD (2019) Extraction of proteins from two marine macroalgae, Ulva sp. and Gracilaria sp., for food application, and evaluating digestibility, amino acid composition and antioxidant properties of the protein concentrates. Food Hydrocoll 87:194–203.  https://doi.org/10.1016/j.foodhyd.2018.07.047 CrossRefGoogle Scholar
  12. Kumaresan M, Vijai Anand K, Govindaraju K, Tamilselvan S, Ganesh Kumar V (2018) Seaweed Sargassum wightii mediated preparation of zirconia (ZrO2) nanoparticles and their antibacterial activity against Gram positive and Gram negative bacteria. Microb Pathog 124:311–315.  https://doi.org/10.1016/j.micpath.2018.08.060 CrossRefGoogle Scholar
  13. Lezcano V, Fernández C, Parodi ER, Morelli S (2018) Antitumor and antioxidant activity of the freshwater macroalga Cladophora surera. J Appl Phycol 30:2913–2921Google Scholar
  14. Li F, Hu H (2005) Isolation and characterization of a novel antialgal allelochemical from Phragmites communis. Society 71:6545–6553.  https://doi.org/10.1128/AEM.71.11.6545 Google Scholar
  15. Li Y, Sun S, Pu X, Yang Y, Zhu F, Zhang S, Xu N (2018) Evaluation of antimicrobial activities of seaweed resources from Zhejiang Coast, China. Sustainability 10:2158.  https://doi.org/10.3390/su10072158 CrossRefGoogle Scholar
  16. Meepagala KM, Schrader KK, Wedge DE, Duke SO (2005) Algicidal and antifungal compounds from the roots of Ruta graveolens and synthesis of their analogs. Phytochemistry 66:2689–2695.  https://doi.org/10.1016/j.phytochem.2005.09.019 CrossRefGoogle Scholar
  17. Mishra AK (2018) Sargassum, Gracilaria and Ulva exhibit positive antimicrobial activity against human pathogens. OALib 05:1–11.  https://doi.org/10.4236/oalib.1104258 Google Scholar
  18. Park MH, Chung IM, Ahmad A, Kim BH, Hwang SJ (2009) Growth inhibition of unicellular and colonial Microcystis strains (Cyanophyceae) by compounds isolated from rice (Oryza sativa) hulls. Aquat Bot 90:309–314.  https://doi.org/10.1016/j.aquabot.2008.11.007 CrossRefGoogle Scholar
  19. Pérez MJ, Falqué E, Domínguez H (2016) Antimicrobial action of compounds from marine seaweed. Mar Drugs 14:1–38.  https://doi.org/10.3390/md14030052 CrossRefGoogle Scholar
  20. Rodrigues D, Freitas AC, Pereira L, Rocha-Santos TAP, Vasconcelos MW, Roriz M, Rodríguez-Alcalá LM, Gomes AMP, Duarte AC (2015) Chemical composition of red, brown and green macroalgae from Buarcos bay in Central West Coast of Portugal. Food Chem 183:197–207.  https://doi.org/10.1016/j.foodchem.2015.03.057 CrossRefGoogle Scholar
  21. Sahnouni F, Benattouche Z, Matallah-Boutiba A et al (2016) Antimicrobial activity of two marine algae Ulva rigida and Ulva intestinalis collected from Arzew gulf (Western Algeria). J Appl Environ Biol Sci 6:242–248Google Scholar
  22. Salvador N, Garreta AG, Lavelli L, Ribera MA (2007) Antimicrobial activity of Iberian macroalgae. Sci Mar 71:101–113.  https://doi.org/10.3989/scimar.2007.71n1101 CrossRefGoogle Scholar
  23. Sbiyyaa B, Loudiki M, Oudra B (1998) Capacité de stockage intracellulaire de l’azote et du phosphore chez Microcystis aeruginosa Kütz. Et Synechocystis sp.: cyanobactéries toxiques occa-sionnant des. Ann Limnol 34:247–257CrossRefGoogle Scholar
  24. Schrader KK (2003) Natural algicides for the control of cyanobacterial-related off-flavor in catfish aquaculture. Off-Flavors Aquac 848:195–208.  https://doi.org/10.1021/bk-2003-0848.ch014 CrossRefGoogle Scholar
  25. Schwartz N, Dobretsov S, Rohde S, Schupp PJ (2017) Comparison of antifouling properties of native and invasive Sargassum (Fucales, Phaeophyceae) species. Eur J Phycol 52:116–131.  https://doi.org/10.1080/09670262.2016.1231345 CrossRefGoogle Scholar
  26. Seder-Colomina M, Burgos A, Maldonado J, Solé A, Esteve I (2013) The effect of copper on different phototrophic microorganisms determined in vivo and at cellular level by confocal laser microscopy. Ecotoxicology 22:199–205.  https://doi.org/10.1007/s10646-012-1014-0 CrossRefGoogle Scholar
  27. Shirai M, Matumaru K, Ohotake A et al (1989) Development of a solid medium for growth and isolation of axenic Microcystis strains (Cyanobacteria). Appl Environ Microbiol 55:2569–2571Google Scholar
  28. Soliman AS, Ahmed AY, Abdel-Ghafour SE et al (2018) Antifungal bio-efficacy of the red algae Gracilaria confervoides extracts against three pathogenic fungi of cucumber plant. Middle East J Appl Sci 08:727–735Google Scholar
  29. Sun X, Jin H, Zhang L, Hu W, Li Y, Xu N (2016a) Screening and isolation of the algicidal compounds from marine green alga Ulva intestinalis. Chin J Oceanol Limnol 34:781–788.  https://doi.org/10.1007/s00343-016-4383-z CrossRefGoogle Scholar
  30. Sun Y y, Wang H, Guo G l et al (2016b) Isolation, purification, and identification of antialgal substances in green alga Ulva prolifera for antialgal activity against the common harmful red tide microalgae. Environ Sci Pollut Res 23:1449–1459.  https://doi.org/10.1007/s11356-015-5377-7 CrossRefGoogle Scholar
  31. Sun Y y, Meng K, Z xia S et al (2017) Isolation and purification of antialgal compounds from the red alga Gracilaria lemaneiformis for activity against common harmful red tide microalgae. Environ Sci Pollut Res 24:4964–4972.  https://doi.org/10.1007/s11356-016-8256-y CrossRefGoogle Scholar
  32. Sun Y y, jing ZW, Wang H et al (2018) Antialgal compounds with antialgal activity against the common red tide microalgae from a green algae Ulva pertusa. Ecotoxicol Environ Saf 157:61–66.  https://doi.org/10.1016/j.ecoenv.2018.03.051 CrossRefGoogle Scholar
  33. Tazart Z, Douma M, Tebaa L, Loudiki M (2018) Use of macrophytes allelopathy in the biocontrol of harmful Microcystis aeruginosa blooms. Water Sci Technol Water Supply.  https://doi.org/10.2166/ws.2018.072
  34. Tebaa L, Douma M, Tazart Z et al (2018) Assessment of the potentially algicidal effects of Thymus satureioides Coss. and Artemisia herba alba L. against Microcystis aeruginosa. Appl Ecol Environ Res 16:903–912.  https://doi.org/10.15666/aeer/1601_903912 CrossRefGoogle Scholar
  35. Visser PM, Ibelings BW, Mur LR, Walsby AE (2005) The ecophysiology of the harmful cyanobacterium Microcystis. Harmful Cyanobacteria 3:109–142.  https://doi.org/10.1007/1-4020-3022-3_6 CrossRefGoogle Scholar
  36. Wang R, Wang Y, Tang X (2012) Identification of the toxic compounds produced by Sargassum thunbergii to red tide microalgae. Chin J Oceanol Limnol 30:778–785Google Scholar
  37. Wang H, Liang F, Zhang L (2015) Composition and anticyanobacterial activity of essential oils from six different submerged macrophytes. Polish J Environ Stud 24:333–338.  https://doi.org/10.15244/pjoes/26383 CrossRefGoogle Scholar
  38. Wang R, Chen J, Ding N, Han M, Wang J, Zhang P, Liu X, Zheng N, Gao P (2018) Antialgal effects of α-linolenic acid on harmful bloom-forming Prorocentrum donghaiense and the antialgal mechanisms. Environ Sci Pollut Res 25:1–9.  https://doi.org/10.1007/s11356-018-2536-7 Google Scholar
  39. Wu ZB, Zhang SH, Wu XH et al (2007) Allelopathic interactions between Potamogelon maackianus and Microcystis aeruginosa. Allelopath J 20:327–338Google Scholar
  40. Xu H, Paerl HW, Qin BQ, Zhu G, Gaoa G (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnol Oceanogr 55:420–432.  https://doi.org/10.4319/lo.2010.55.1.0420 CrossRefGoogle Scholar
  41. Zerrif SEA, El Ghazi N, Douma M et al (2018) Potential uses of seaweed bioactive compounds for harmful microalgae blooms control: algicidal effects and algal growth inhibition of Phormidium sp. (freshwater toxic cyanobacteria). Smetox J 1:59–62Google Scholar
  42. Zerrifi SEA, El KF, Oudra B, Vasconcelos V (2018) Seaweed bioactive compounds against pathogens and microalgae: potential uses on pharmacology and harmful algae bloom control. Mar Drugs 16.  https://doi.org/10.3390/md16020055
  43. Zhu J, Liu B, Wang J, Gao Y, Wu Z (2010) Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquat Toxicol 98:196–203.  https://doi.org/10.1016/j.aquatox.2010.02.011 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Biology and Biotechnology of Microorganisms, Faculty of Sciences Semlalia MarrakechCadi Ayyad UniversityMarrakechMorocco
  2. 2.Polydisciplinary Faculty of Khouribga (FPK)Sultan Moulay Slimane UniversityBeni-MellalMorocco
  3. 3.CIIMAR, Interdisciplinary Centre of Marine and Environmental ResearchTerminal de Cruzeiros do Porto de LeixõesMatosinhosPortugal
  4. 4.Departament of Biology, Faculty of SciencesUniversity of PortoPortoPortugal

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