Antifungal activity of microalgae in phytopathogenic fungi: A systematic review
DOI:
https://doi.org/10.5902/2179460X84584Keywords:
Agriculture, Antifungal activity, Phytopathogens, Fungi, MicroalgaeAbstract
Phytopathogenic fungi are a group of organisms that cause diseases in plants through disturbances in their cellular metabolism. They have major impacts on agriculture, accounting for 8 - 40% of the losses in world agricultural production. Meanwhile, microalgae synthesize a wide variety of allelopathic chemicals and can be used for different biocidal purposes, including antifungal. The objective of this study was to review the antifungal activity of microalgal extracts and their compounds against phytopathogenic fungi. This systematic review of the literature was conducted using SciELO, PubMed, and Periódicos Capes (Scopus). Following the search, 25 articles published in English and Portuguese were selected. Several publications will be recorded from 2015 to 2022. Eight microalgal phyla (Bacillariophyta, Chlorophyta, Cyanobacteria, Haptophyta, Miozoa, Ochrophyta, Prasinodermatophyta, and Rhodophyta) were detected, with Chlorophyta and Cyanobacteria having the highest number of registered publications. The most tested species of phytopathogenic fungi were Aspergillus niger and Botrytis cinerea. Regarding the categorized inhibition classification for the assays, high inhibition was observed in 31.26% of the trials. Studies performed with cyanobacterial species showed a higher proportion of high inhibition (41.36%) of phytopathogens. Given the high degree of biodiversity of microalgae and their wide range of associated bioactive molecules, this is a vast field to explore for novel biopesticides with antifungal potential.
Downloads
References
Alvarez A.L., Weyers S.L., Goemann H.M., Peyton B.M., Gardner R.D. (2021) Microalgae, soil and plants: A critical review of microalgae as renewable resources for agriculture. Algal Res. https://doi.org/10.1016/j.algal.2021.102200
Anees M., Edel-Hermann V., Steinberg C. (2010) Buildup of patches caused by Rhizoctonia solani. Soil Biol Biochem. https://doi.org/10.1016/j.soilbio.2010.05.013
Archibaldi J.M., Simpson A.G.B., Slamovits C.H. (2017) Handbook of the Protists. Springer, Boston. https://doi.org/10.1007/978-3-319-28149-0
Balouiri M., Sadiki M., Ibnsouda S.K. (2016) Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal. https://doi.org/10.1016/j.jpha.2015.11.005
Bashir K.M.I., Lee J.H., Petermann M.J., et al. (2018) Estimation of Antibacterial Properties of Chlorophyta, Rhodophyta and Haptophyta Microalgae Species. Microbiol Biotechnol Lett. https://doi.org/10.4014/mbl.1802.02015
Baudelet P.H., Ricochon G., Linder M., Muniglia L. (2017) A new insight into cell walls of Chlorophyta. Algal Res. https://doi.org/10.1016/j.algal.2017.04.008
Bowles A.M.C., Williamson C.J., Williams T.A., Lenton T.M., Donoghue P.C.J. (2022) The origin and early evolution of plants. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2022.09.009
Brauer V.S., Rezende C.P., Pessoni A.M., et al. (2019) Antifungal Agents in Agriculture: Friends and Foes of Public Health. Biomolecules. https://doi.org/10.3390/biom9100521
Carneiro M., Ranglová K., Lakatos G.E., et al. (2021) Growth and bioactivity of two chlorophyte (Chlorella and Scenedesmus) strains co-cultured outdoors in two different thin-layer units using municipal wastewater as a nutrient source. Algal Res. https://doi.org/10.1016/j.algal.2021.102299
Cepas V., Del-Rio I.G., López Y., et al. (2021) Microalgae and Cyanobacteria Strains as Producers of Lipids with Antibacterial and Antibiofilm Activity. Mar Drugs. https://doi.org/10.3390/md19120675
Chandrasekaran M., Thangavelu B., Chun S.C., Sathiyabama M. (2016) Proteases from phytopathogenic fungi and their importance in phytopathogenicity. J Gen Plant Pathol. https://doi.org/10.1007/s10327.016.0672-9
Costa J.A.V., Freitas B.C.B., Cruz C.G., Silveira J., Morais M.G. (2019) Potential of microalgae as biopesticides to contribute to sustainable agriculture and environmental development. J Environ Sci Health. https://doi.org/10.1080/03601.234.2019.1571366
Costa J.A.V., Cassuriaga A.P.A., Moraes L., Morais M.G. (2022) Biosynthesis and potential applications of terpenes produced from microalgae. Bioresour Technol Rep. https://doi.org/10.1016/j.biteb.2022.101166
Davoodbasha M., Edachery B., Nooruddin T., Lee S.Y., Kim J.W. (2018) An evidence of C16 fatty acid methyl esters extracted from microalga for effective antimicrobial and antioxidant property. Microb Pathog. https://doi.org/10.1016/j.micpath.2017.12.049
Dean R., Kan J.A.L.V., Pretorius Z.A., et al. (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. https://doi.org/10.1111/j.1364-3703.2011.00783.x
El Semary N.A., Mabrouk M. (2013) Molecular characterization of two microalgal strains in Egypt and investigation of the antimicrobial activity of their extracts. Biotechnol Agron Soc Environ 17:312-320
Fábregas J., García D., Fernandez-Alonso M., et al. (1999) In vitro inhibition of the replication of haemorrhagic septicaemia virus (VHSV) and African swine fever virus (ASFV) by extracts from marine microalgae. Antivir Res. https://doi.org/10.1016/S0166-3542(99)00049-2
Falaise C., François C., Travers M.A., et al. (2016) Antimicrobial Compounds from Eukaryotic Microalgae against Human Pathogens and Diseases in Aquaculture. Mar Drugs. https://doi.org/10.3390/md14090159
Gallardo-Rodríguez J., Sánchez-Mirón A., García-Camacho F., López-Rosales L., Chisti Y., Molina-Grima E. (2012) Bioactives from microalgal dinoflagellates. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2012.07.005
Hermawan I., Higa M., Hutabarat P.U.B., et al. (2019) Kabirimine, a New Cyclic Imine from an Okinawan Dinoflagellate. Mar Drugs. https://doi.org/10.3390/md17060353
Herrero M., Ibáñez E., Cifuentes A., Reglero G., Santoyo S. (2006) Dunaliella salina Microalga Pressurized Liquid Extracts as Potential Antimicrobials. J Food Prot. https://doi.org/10.4315/0362-028X-69.10.2471
Kashif S.A., Hwang Y.J., Park J.K. (2018) Potent biomedical applications of isolated polysaccharides from marine microalgae Tetraselmis species. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449.018.1987-z
Kaur L. (2019) A review: Top ten fungal pathogens. Int J Res Anal 6:532-542.
Khan M., Salman M., Jan S.A., Shinwari Z.K. (2021) Biological control of fungal phytopathogens: A comprehensive review based on
Bacillus species. MOJ Biol Med. https://doi.org/10.15406/mojbm.2021.06.00137
Kumar J., Ramlal A., Mallick D., Mishra V. (2021) An Overview of Some Biopesticides and Their Importance in Plant Protection for Commercial Acceptance. Plants. https://doi.org/10.3390/plants10061185
Lage V.M.G.B., Deegan K.R., Santos G.F., Barbosa C.J., Lima S.T.C. (2022) Biological activity of microalgae in dermatophytes: Review. Res Soc Dev. https://doi.org/10.33448/rsd-v11i11.33404
Leannec-Rialland V., Atanasova V., Chereau S., Tonk-Rügen M., Cabezas-Cruz A., Richard-Forget F. (2022) Use of Defensins to Develop
Eco-Friendly Alternatives to Synthetic Fungicides to Control Phytopathogenic Fungi and Their Mycotoxins. J Fungi. https://doi.org/10.3390/jof8030229
Martínez K.A., Lauritano C., Druka D., et al. (2019) Amphidinol 22, a New Cytotoxic and Antifungal Amphidinol from the Dinoflagellate Amphidinium carterae. Mar Drugs. https://doi.org/10.3390/md17070385
Mishra J., Arora N.K. (2018) Secondary metabolites of fluorescent pseudomonads in biocontrol of phytopathogens for sustainable agriculture. Appl Soil Ecol. https://doi.org/10.1016/j.apsoil.2017.12.004
Montalvão S., Demirel Z., Devi B., et al. (2016) Large-scale bioprospecting of cyanobacteria, micro – and macroalgae from the Aegean Sea. N Biotechnol. https://doi.org/10.1016/j.nbt.2016.02.002
Morales-Jiménez M., Gouveia L., Yáñez-Fernández J., Castro-Muñoz R., Barragán-Huerta B.E. (2020) Production, Preparation and Characterization of Microalgae-Based Biopolymer as a Potential Bioactive Film. Coatings. https://doi.org/10.3390/coatings10020120
Murata M.M., Morioka L.R.I., Marques J.B.S., Bosso A., Suguimoto H.H. (2021) What do patents tell us about microalgae in agriculture? AMB Express. https://doi.org/10.1186/s13568.021.01315-4
Nabout J.C., Rocha B.S., Carneiro F.M., Sant’Anna C.L. (2013) How many species of Cyanobacteria are there? Using a discovery curve to predict the species number. Biodivers Conserv. https://doi.org/10.1007/s10531.013.0561-x
Najdenski H.M., Gigova L.G., Iliev I.I., et al. (2013) Antibacterial and antifungal activities of selected microalgae and cyanobacteria. Int J Food Sci Technol. https://doi.org/10.1111/ijfs.12122
Neto A.C.R., Souza L.S., Angelo E., et al. (2015) Atividade antimicrobiana de extratos etanólicos de algas no controle de Penicillium expansum Link (Trichocomaceae, Ascomycota). Biotemas. https://doi.org/10.5007/2175-7925.2015v28n4p23
Omran B.A., Baek K.H. (2022) Control of phytopathogens using sustainable biogenic nanomaterials: Recent perspectives, ecological safety, and challenging gaps. J Clean Prod. https://doi.org/10.1016/j.jclepro.2022.133729
Ons L., Bylemans D., Thevissen K., Cammue B.P.A. (2020) Combining Biocontrol Agents with Chemical Fungicides for Integrated Plant Fungal Disease Control. Microorganisms. https://doi.org/10.3390/microorganisms8121930
Patil L., Kaliwal B.B. (2019) Microalga Scenedesmus bajacalifornicus BBKLP-07, a new source of bioactive compounds with in vitro pharmacological applications. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449.019.02099-5
Pawar S.T., Puranik P.R. (2008) Screening of terrestrial and freshwater halotolerant cyanobacteria for antifungal activities. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274.007.9565-6
Peraman M., Nachimuthu S. (2019) Identification and Quantification of Fucoxanthin in Selected Carotenoid-Producing Marine Microalgae and Evaluation for their Chemotherapeutic Potential. Pharmacogn Mag 15:243-249
Perrone G., Susca A., Cozzi G., et al. (2007) Biodiversity of Aspergillus species in some important agricultural products. Stud Mycol. https://doi.org/10.3114/sim.2007.59.07
Qasem W.M.A., Mohamed E.A., Hamed A.A., El-Sayed A.E.B., El-Din R.A.S. (2016) Antimicrobial and Anticancer Activity of Some Microalgae Species. Egypt J Phycol. https://doi.org/10.21608/egyjs.2016.115978
Ranglová K., Lakatos G.E., Manoel J.A.C., et al. (2021) Growth, biostimulant and biopesticide activity of the MACC-1 Chlorella strain cultivated outdoors in inorganic medium and wastewater. Algal Res. https://doi.org/10.1016/j.algal.2020.102136
Righini H., Francioso O., Di Foggia M., Quintana A.M., Roberti R. (2021) Assessing the Potential of the Terrestrial Cyanobacterium Anabaena minutissima for Controlling Botrytis cinerea on Tomato Fruits. Horticulturae. https://doi.org/10.3390/horticulturae7080210
Righini H., Francioso O., Di Foggia M., Quintana A.M., Roberti R. (2020) Preliminary Study on the Activity of Phycobiliproteins against Botrytis cinerea. Mar Drugs. https://doi.org/10.3390/md18120600
Righini H., Francioso O., Quintana A.M., Roberti R. (2022) Cyanobacteria: A Natural Source for Controlling Agricultural Plant Diseases Caused by Fungi and Oomycetes and Improving Plant Growth. Horticulture. https://doi.org/10.3390/horticulturae8010058
Rio-Garati A.D., Garcia-Mosaica C. (2022) Antimicrobial activity of marine microalgae: Isochrysis galbana, Isochrysis litoralis and Isochrysis maritima. J Anal Sci Appl Biotechnol. https://doi.org/10.48402/IMIST.PRSM/jasab-v4i2.39137
Rodríguez-Meizoso I., Jaime L., Santoyo S., et al. (2008) Pressurized Fluid Extraction of Bioactive Compounds from Phormidium Species. J Agric Food Chem. https://doi.org/10.1021/jf703719p
Saeed M.U., Hussain N., Shahbaz A., Hameed T., Iqbal H.M.N., Bilal M. (2022) Bioprospecting microalgae and cyanobacteria for biopharmaceutical applications. J Basic Microbiol. https://doi.org/10.1002/jobm.202100445
Santoyo S., Rodríguez-Meizoso I., Cifuentes A., et al. (2009) Green processes based on the extraction with pressurized fluids to obtain potent antimicrobials from Haematococcus pluvialis microalgae. LWT – Food Sci Technol. https://doi.org/10.1016/j.lwt.2009.01.012
Satake M., Cornelio K., Hanashima S., et al. (2017) Structures of the Largest Amphidinol Homologues from the Dinoflagellate Amphidinium carterae and Structure–Activity Relationships. J Nat Prod. https://doi.org/10.1021/acs.jnatprod.7b00345
Scaglioni P.T., Garcia S.O., Badiale-Furlong E. (2019) Inhibition of in vitro trichothecenes production by microalgae phenolic extracts. Food Res Int. https://doi.org/10.1016/j.foodres.2018.07.008
Scaglioni P.T., Pagnussatt F.A., Lemos A.C., Nicolli C.P., Del Ponte E.M., BadialeFurlong E. (2019) Nannochloropsis sp. and Spirulina sp. as a Source of Antifungal Compounds to Mitigate Contamination by Fusarium graminearum Species Complex. Curr Microbiol.
https://doi.org/10.1007/s00284.019.01663-2
Schmid B., Coelho L., Schulze P.S.C., et al. (2022) Antifungal properties of aqueous microalgal extracts. Bioresour Technol Rep.
https://doi.org/10.1016/j.biteb.2022.101096
Senousy H.H., El-Sheekh M.M., Saber A.A., et al. (2022) Biochemical Analyses of Ten Cyanobacterial and Microalgal Strains Isolated from Egyptian Habitats, and Screening for Their Potential against Some Selected Phytopathogenic Fungal Strains. Agronomy. https://doi.org/10.3390/agronomy12061340
Sexton J.P., Lomas M.W. (2018) Microalgal Systematics. In: Levine I, Fleurence J (eds) Microalgae in Health and Disease Prevention. Academic Press, Cambridge, pp 73-107
Silberfeld T., Rousseau F., Reviers B. (2014) An updated classification of brown algae (Ochrophyta, Phaeophyceae). Algologie. https://doi.org/10.7872/crya.v35.iss2.2014.117
Stirk W.A., Staden J. (2022) Bioprospecting for bioactive compounds in microalgae: Antimicrobial compounds. Biotechnol Adv. https://doi.org/10.1016/j.biotechadv.2022.107977
Sun J., Zhao J., Fu D., Gu S., Wang D. (2017) Extraction, Optimization and Antimicrobial Activity of IWSP from Oleaginous Microalgae Chlamydomonas sp. YB-204. Food Sci Technol Res. https://doi.org/10.3136/fstr.23.819
Suresh A., Praveenkumar R., Thangaraj R., et al. (2014) Microalgal fatty acid methyl ester a new source of bioactive compounds with antimicrobial activity. Asian Pac J Trop Dis. https://doi.org/10.1016/S2222-1808(14)60769-6
Torres-Bayona C., Rojas J.L., Fernandez R., Prieto-Guevara M., Pulido A., Moreno-Garrido I. (2023) Microalgae and Cyanobacteria, a Promising Source of Antimicrobial Molecules Against Aquatic Pathogen. Turkish J Fish Aquat Sci. https://doi.org/10.4194/TRJFAS21184
Vehapi M., Koçer A.T., Yılmaz A., Özçimen D. (2019) Investigation of the antifungal efects of algal extracts on appleinfecting fungi. Arch Microbiol. https://doi.org/10.1007/s00203.019.01760-7
Verweij P.E., Arendrup M.C., Alastruey-Izquierdo A., et al. (2022) Dual use of antifungals in medicine and agriculture: How do we help prevent resistance developing in human pathogens? Drug Resist Updat. https://doi.org/10.1016/j.drup.2022.100885
Vicente T.F.L., Lemos M.F.L., Félix R., Valentão P., Félix C. (2021) Marine Macroalgae, a Source of Natural Inhibitors of Fungal Phytopathogens. J Fungi. https://doi.org/10.3390/jof7121006
Washida K., Koyama T., Yamada K., Kita M., Uemura D. (2006) Karatungiols A and B, two novel antimicrobial polyol compounds, from the symbiotic marine dinoflagellate Amphidinium sp. Tetrahedron Lett. https://doi.org/10.1016/j.tetlet.2006.02.045
Yanuhar U., Nurdiani R., Hertika A.M.S. (2011) Potency of Nannochloropsis oculata as Antibacterial, Antioxidant and Antiviral on Humpback Grouper Infected by Vibrio alginolyticus and Viral Nervous Necrotic. J Food Sci Eng 5:323-330
Yim J.H., Kim S.J., Ahn S.H., Lee C.K., Rhie K.T., Lee H.K. (2004) Antiviral effects of sulfated exopolysaccharide from the marine microalga Gyrodinium impudicum strain KG03. Mar Biotechnol. https://doi.org/10.1007/s10126.003.0002-z
Zahra Z., Choo D.H., Lee H., Parveen A. (2020) Cyanobacteria: Review of current potentials and applications. Environments. https://doi.org/10.3390/environments7020013
Zielinski D., Fraczyk J., Debowski M., et al. (2020) Biological Activity of Hydrophilic Extract of Chlorella vulgaris Grown on Post-Fermentation Leachate from a Biogas Plant Supplied with Stillage and Maize Silage. Molecules. https://doi.org/10.3390/molecules25081790
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Ciência e Natura
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
To access the DECLARATION AND TRANSFER OF COPYRIGHT AUTHOR’S DECLARATION AND COPYRIGHT LICENSE click here.
Ethical Guidelines for Journal Publication
The Ciência e Natura journal is committed to ensuring ethics in publication and quality of articles.
Conformance to standards of ethical behavior is therefore expected of all parties involved: Authors, Editors, Reviewers, and the Publisher.
In particular,
Authors: Authors should present an objective discussion of the significance of research work as well as sufficient detail and references to permit others to replicate the experiments. Fraudulent or knowingly inaccurate statements constitute unethical behavior and are unacceptable. Review Articles should also be objective, comprehensive, and accurate accounts of the state of the art. The Authors should ensure that their work is entirely original works, and if the work and/or words of others have been used, this has been appropriately acknowledged. Plagiarism in all its forms constitutes unethical publishing behavior and is unacceptable. Submitting the same manuscript to more than one journal concurrently constitutes unethical publishing behavior and is unacceptable. Authors should not submit articles describing essentially the same research to more than one journal. The corresponding Author should ensure that there is a full consensus of all Co-authors in approving the final version of the paper and its submission for publication.
Editors: Editors should evaluate manuscripts exclusively on the basis of their academic merit. An Editor must not use unpublished information in the editor's own research without the express written consent of the Author. Editors should take reasonable responsive measures when ethical complaints have been presented concerning a submitted manuscript or published paper.
Reviewers: Any manuscripts received for review must be treated as confidential documents. Privileged information or ideas obtained through peer review must be kept confidential and not used for personal advantage. Reviewers should be conducted objectively, and observations should be formulated clearly with supporting arguments, so that Authors can use them for improving the paper. Any selected Reviewer who feels unqualified to review the research reported in a manuscript or knows that its prompt review will be impossible should notify the Editor and excuse himself from the review process. Reviewers should not consider manuscripts in which they have conflicts of interest resulting from competitive, collaborative, or other relationships or connections with any of the authors, companies, or institutions connected to the papers.
