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.
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References
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
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
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
Begum S, Nyandoro S, Buriyo A et al (2018) Bioactivities of extracts, debromolaurinterol and fucosterol from macroalgae species. Tanzania J Sci 44:104–116
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
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
Demeke A (2016) Cyanobacteria blooms and biological control. Methods 3:32–38
Gao L, Xie L (2011) Analysis of the influence of meteorological condition on cyanobacterial bloom and treatment methods in Taihu Lake. China Resour 29:35–38
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
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
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
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
Lezcano V, Fernández C, Parodi ER, Morelli S (2018) Antitumor and antioxidant activity of the freshwater macroalga Cladophora surera. J Appl Phycol 30:2913–2921
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
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
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
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
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
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
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
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 6:242–248
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
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 34:247–257
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
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
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
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 55:2569–2571
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 08:727–735
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
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
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
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
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
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
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
Wang R, Wang Y, Tang X (2012) Identification of the toxic compounds produced by Sargassum thunbergii to red tide microalgae. Chin J Oceanol Limnol 30:778–785
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
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
Wu ZB, Zhang SH, Wu XH et al (2007) Allelopathic interactions between Potamogelon maackianus and Microcystis aeruginosa. Allelopath J 20:327–338
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
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 1:59–62
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
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
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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),
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El Amrani Zerrifi, S., Tazart, Z., El Khalloufi, F. et al. Potential control of toxic cyanobacteria blooms with Moroccan seaweed extracts. Environ Sci Pollut Res 26, 15218–15228 (2019). https://doi.org/10.1007/s11356-019-04921-9
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DOI: https://doi.org/10.1007/s11356-019-04921-9