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Volume 165, Issue 6

A review of allelopathy on microalgae Free

Abstract

Algal blooms have severe impacts on the utilization of water resources. The discovery of allelopathy provides a new dimension to solving this problem due to its high efficiency, safety and economy. Allelopathy can suppress the growth of microalgae by impairing the structure, photosynthesis and enzyme activity of algal cells. In the current work, we first demonstrate the allelopathy and allelochemicals derived from both plants and algae. We then expound the potential mechanisms of allelopathy on microalgae. Next, the potential application of allelochemicals in water environment is proposed. Finally, the key challenge and future perspective are presented.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): allelochemical , allelopathy , allelopathy mechanism , Microalgae and potential application
© 2019 The Authors
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2019-01-28
2024-04-25
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References

  1. Fx F, Tatters AO, Hutchins DA. Global change and the future of harmful algal blooms in the ocean. Marine Ecology Progress 2012; 470:207–233
     [Google Scholar]
  2. Visser PM, Verspagen JMH, Sandrini G, Stal LJ, Matthijs HCP et al. How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae 2016; 54:145–159 [View Article][PubMed]
     [Google Scholar]
  3. Ma Z, Fang T, Thring RW, Li Y, Yu H et al. Toxic and non-toxic strains of Microcystis aeruginosa induce temperature dependent allelopathy toward growth and photosynthesis of Chlorella vulgaris. Harmful Algae 2015; 48:21–29 [View Article][PubMed]
     [Google Scholar]
  4. Li FM, Hu HY. Isolation and characterization of a novel antialgal allelochemical from Phragmites communis. Appl Environ Microbiol 2005; 71:6545–6553 [View Article][PubMed]
     [Google Scholar]
  5. Testai E, Scardala S, Vichi S, Buratti FM, 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 [View Article][PubMed]
     [Google Scholar]
  6. Zheng G, Xu R, Chang X, Hilt S, Wu C. Cyanobacteria can allelopathically inhibit submerged macrophytes: Effects of Microcystis aeruginosa extracts and exudates on Potamogeton malaianus. Aquatic Botany 2013; 109:1–7 [View Article]
     [Google Scholar]
  7. Hamilton TJ, Paz-Yepes J, Morrison RA, Palenik B, Tresguerres M. Exposure to bloom-like concentrations of two marine Synechococcus cyanobacteria (strains CC9311 and CC9902) differentially alters fish behaviour. Conserv Physiol 2014; 2:1–9 [View Article][PubMed]
     [Google Scholar]
  8. Żak A, Kosakowska A. Allelopathic influence of cyanobacteria Microcystis aeruginosa on green algae Chlorella vulgaris. Geoplanet Earth & Planetary Sciences 2014; 14:141–150
     [Google Scholar]
  9. Gentien P, Fukuyo Y, Anderson DM, Blackburn S, Cembella A et al. Global ecology and oceanography of harmful algal blooms. Scor & Ioc 2001
     [Google Scholar]
  10. Lou X, Hu C. Diurnal changes of a harmful algal bloom in the East China Sea: Observations from GOCI. Remote Sens Environ 2014; 140:562–572 [View Article]
     [Google Scholar]
  11. Gavrilović BR, Despotović SG, Gavrić JP, Borković-Mitić SS, Ognjanović BI et al. Changes in antioxidant enzyme activities in the livers and gills of three cyprinids after exposure to a cyanobacterial bloom in the Gruža Reservoir, Serbia. Ecol Indic 2014; 38:141–148 [View Article]
     [Google Scholar]
  12. Lundgren VM, Roelke DL, Grover JP, Brooks BW, Prosser KN et al. Interplay between ambient surface water mixing and manipulated hydraulic flushing: Implications for harmful algal bloom mitigation. Ecol Eng 2013; 60:289–298 [View Article]
     [Google Scholar]
  13. Anderson DM. Turning back the harmful red tide. Nature 1997; 388:513–514 [View Article]
     [Google Scholar]
  14. Hoko Z, Makado PK. Optimization of algal removal process at Morton Jaffray water works, Harare, Zimbabwe. Phys Chem Earth 2011; 36:1141–1150 [View Article]
     [Google Scholar]
  15. Vyvyan JR. ChemInform Abstract: Allelochemicals as Leads for New Herbicides and Agrochemicals. ChemInform 2002; 33:1631–1646 [View Article]
     [Google Scholar]
  16. Nakai S, Inoue Y, Hosomi M. Algal growth inhibition effects and inducement modes by plant-producing phenols. Water Res 2001; 35:1855–1859 [View Article][PubMed]
     [Google Scholar]
  17. Rice EL. Allelopathy Academic Press; 1984
     [Google Scholar]
  18. Zhai MP. Allelopathy of forest plants. J Beijing Forestry Univ 1993
     [Google Scholar]
  19. Olofsdotter M. Allelopathy in rice. Allelopathy in Rice 1996
     [Google Scholar]
  20. Hong Y, Hu HY, Xie X, Sakoda A, Sagehashi M et al. Gramine-induced growth inhibition, oxidative damage and antioxidant responses in freshwater cyanobacterium Microcystis aeruginosa. Aquat Toxicol 2009; 91:262–269 [View Article][PubMed]
     [Google Scholar]
  21. Nakai S. Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Res 2000; 34:3026–3032 [View Article]
     [Google Scholar]
  22. Nakai S, Yamada S, Hosomi M. Anti-cyanobacterial fatty acids released from Myriophyllum spicatum. Hydrobiologia 2005; 543:71–78 [View Article]
     [Google Scholar]
  23. Zi J, Mafu S, Peters RJ. To gibberellins and beyond! Surveying the evolution of (di)terpenoid metabolism. Annu Rev Plant Biol 2014; 65:259–286 [View Article][PubMed]
     [Google Scholar]
  24. Weston LA, Mathesius U. Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 2013; 39:283–297 [View Article][PubMed]
     [Google Scholar]
  25. Körner S. Loss of Submerged Macrophytes in Shallow Lakes in North-Eastern Germany. Int Rev Hydrobiol 2002; 87:375–384 [View Article]
     [Google Scholar]
  26. Gao YN, Liu BY, Xu D, Zhou QH, Cy H et al. Phenolic compounds exuded from two submerged freshwater macrophytes and their allelopathic effects on Microcystis aeruginosa. Pol J Environ Stud 2011; 20:1153–1159
     [Google Scholar]
  27. Gao YN, Liu BY, Fj G, He Y, Zy L et al. Joint effects of allelochemical nonanoic acid, n-phenyl-1-naphtylamine and caffeic acid on the growth of microcystis aeruginosa. Allelopathy Journal 2015; 35:249–258
     [Google Scholar]
  28. Nakai S, Zou G, Okuda T, Nishijima W, Hosomi M et al. Polyphenols and fatty acids responsible for anti-cyanobacterial allelopathic effects of submerged macrophyte Myriophyllum spicatum. Water Sci Technol 2012; 66:993–999 [View Article][PubMed]
     [Google Scholar]
  29. Zy L, Liu BY, He Y, Chen ZL, Zhou QH et al. Effects of daily exposure of cyanobacterium and chlorophyte to low-doses of pyrogallol. Allelopathy Journal 2014; 34:195–205
     [Google Scholar]
  30. Gao YN, Ge FJ, Zhang LP, He Y, Lu ZY et al. Enhanced toxicity to the cyanobacterium Microcystis aeruginosa by low-dosage repeated exposure to the allelochemical N-phenyl-1-naphthylamine. Chemosphere 2017; 174:732–738 [View Article][PubMed]
     [Google Scholar]
  31. Zhang T, Zheng C, He M, Wu A, Nie L. Inhibition on algae of fatty acids and the structure-effect relationship. China Environmental Science 2009; 29:274–279
     [Google Scholar]
  32. Nakai S, Asaoka S, Okuda T, Nishijima W. Growth Inhibition of Microcystis aeruginosa by Allelopathic Compounds Originally Isolated from Myriophyllum spicatum: Temperature and Light Effects and Evidence of Possible Major Mechanisms. J Chem Eng Jpn 2014; 47:488–493 [View Article]
     [Google Scholar]
  33. Inderjit, Dakshini KMM. Algal allelopathy. Botanical Review 1994; 60:182–196 [View Article]
     [Google Scholar]
  34. Fergola P, Cerasuolo M, Pollio A, Pinto G, Dellagreca M. Allelopathy and competition between Chlorella vulgaris and Pseudokirchneriella subcapitata: Experiments and mathematical model. Ecol Modell 2007; 208:205–214 [View Article]
     [Google Scholar]
  35. Shao J, Peng L, Luo S, Yu G et al. First report on the allelopathic effect of Tychonema bourrellyi (Cyanobacteria) against Microcystis aeruginosa (Cyanobacteria). J Appl Phycol 2013; 25:1567–1573 [View Article]
     [Google Scholar]
  36. Rzymski P, Poniedziałek B, Kokociński M, Jurczak T, Lipski D et al. Interspecific allelopathy in cyanobacteria: Cylindrospermopsin and Cylindrospermopsis raciborskii effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae 2014; 35:1–8 [View Article]
     [Google Scholar]
  37. Wang L, Zi J, Xu R, Hilt S, Hou X et al. Allelopathic effects of Microcystis aeruginosa on green algae and a diatom: Evidence from exudates addition and co-culturing. Harmful Algae 2017; 61:56–62 [View Article]
     [Google Scholar]
  38. Gantar M, Berry JP, Thomas S, Wang M, Perez R et al. Allelopathic activity among Cyanobacteria and microalgae isolated from Florida freshwater habitats. FEMS Microbiol Ecol 2008; 64:55–64 [View Article][PubMed]
     [Google Scholar]
  39. Gross EM. Allelopathy of Aquatic Autotrophs. CRC Crit Rev Plant Sci 2003; 22:313–339 [View Article]
     [Google Scholar]
  40. Leão PN, Pereira AR, Liu WT, Ng J, Pevzner PA et al. Synergistic allelochemicals from a freshwater cyanobacterium. Proc Natl Acad Sci USA 2010; 107:11183–11188 [View Article][PubMed]
     [Google Scholar]
  41. Dellagreca M, Zarrelli A, Fergola P, Cerasuolo M, Pollio A et al. Fatty acids released by Chlorella vulgaris and their role in interference with Pseudokirchneriella subcapitata: experiments and modelling. J Chem Ecol 2010; 36:339–349 [View Article][PubMed]
     [Google Scholar]
  42. Leflaive, Ten-Hage L. Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshw Biol 2007; 52:199–214 [View Article]
     [Google Scholar]
  43. Larkum AWD, Douglas SE, Raven JA. Photosynthesis in algae Springer; 2003
     [Google Scholar]
  44. Fm L, Hy H, Chong YX, Men YJ, Guo MT. Influence of EMA isolated from Phragmites communis on physiological characters of Microcystis aeruginosa. China Environmental Science 2007; 27:377–381
     [Google Scholar]
  45. Qian H, Xu X, Chen W, Jiang H, Jin Y et al. Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 2009; 75:368–375 [View Article][PubMed]
     [Google Scholar]
  46. Zhu J, Liu B, Wang J, Gao Y, Wu Z. Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquat Toxicol 2010; 98:196–203 [View Article][PubMed]
     [Google Scholar]
  47. Gleason FK. The natural herbicide, cyanobacterin, specifically disrupts thylakoid membrane structure in Euglena gracilis strain Z. FEMS Microbiol Lett 1990; 68:77–81 [View Article]
     [Google Scholar]
  48. Srivastava A, Jüttner F, Strasser RJ. Action of the allelochemical, fischerellin A, on photosystem II. Biochim Biophys Acta 1998; 1364:326–336 [View Article][PubMed]
     [Google Scholar]
  49. Xin L, Hong-Ying H, Jia Y, Yin-Hu W. Enhancement effect of ethyl-2-methyl acetoacetate on triacylglycerols production by a freshwater microalga, Scenedesmus sp. LX1. Bioresour Technol 2010; 101:9819–9821 [View Article][PubMed]
     [Google Scholar]
  50. Li FM, Hu HY, Chong YX, Men YJ, Guo MT. [Effects of allelochemical EMA isolated from Phragmites communis on algal cell membrane lipid and ultrastructure]. Huan Jing Ke Xue 2007; 28:1534–1538[PubMed]
     [Google Scholar]
  51. Sun X-X, Choi J-K, Kim E-K. A preliminary study on the mechanism of harmful algal bloom mitigation by use of sophorolipid treatment. J Exp Mar Bio Ecol 2004; 304:35–49 [View Article]
     [Google Scholar]
  52. Hong Y, Hu HY, Xie X, Li FM. Responses of enzymatic antioxidants and non-enzymatic antioxidants in the cyanobacterium Microcystis aeruginosa to the allelochemical ethyl 2-methyl acetoacetate (EMA) isolated from reed (Phragmites communis). J Plant Physiol 2008; 165:1264–1273 [View Article][PubMed]
     [Google Scholar]
  53. Mohamed ZA, Al Shehri AM. Differential Responses of Epiphytic and Planktonic Toxic Cyanobacteria to Allelopathic Substances of the Submerged Macrophyte Stratiotes aloides. Int Rev Hydrobiol 2010; 95:224–234 [View Article]
     [Google Scholar]
  54. Durrant JR, Giorgi LB, Barber J, Klug DR, Porter G. Characterisation of triplet states in isolated Photosystem II reaction centres: Oxygen quenching as a mechanism for photodamage. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1990; 1017:167–175 [View Article]
     [Google Scholar]
  55. Vardi A, Formiggini F, Casotti R, de Martino A, Ribalet F et al. A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biol 2006; 4:411–419 [View Article][PubMed]
     [Google Scholar]
  56. Zhang T-T, Zheng C-Y, Hu W, Xu W-W, Wang H-F. The allelopathy and allelopathic mechanism of phenolic acids on toxic Microcystis aeruginosa. J Appl Phycol 2010; 22:71–77 [View Article]
     [Google Scholar]
  57. Wink M, Latz-Brüning B. Allelopathic Properties of Alkaloids and Other Natural Products 1995
     [Google Scholar]
  58. Wink M, Schmeller T, Latz-Brüning B. Modes of action of allelochemical alkaloids: Interaction with neuroreceptors, DNA, and other molecular targets. J Chem Ecol 1998; 24:1881–1937 [View Article]
     [Google Scholar]
  59. Shao J, Yu G, Wang Z, Wu Z, Peng X et al. Towards clarification of the inhibitory mechanism of wheat bran leachate on Microcystis aeruginosa NIES-843 (Cyanobacteria): physiological responses. Ecotoxicology 2010; 19:1634–1641 [View Article][PubMed]
     [Google Scholar]
  60. Jacques S, Ghesquière B, van Breusegem F, Gevaert K. Plant proteins under oxidative attack. Proteomics 2013; 13:932–940 [View Article][PubMed]
     [Google Scholar]
  61. Choi RC, Jiang Z, Xie HQ, Cheung AW, Lau DT et al. Anti-oxidative effects of the biennial flower of Panax notoginseng against H2O2-induced cytotoxicity in cultured PC12 cells. Chin Med 2010; 5:38 [View Article][PubMed]
     [Google Scholar]
  62. Usenko OM, Guseynova VP, Sakevich AI. Peculiarities of the Influence of Polyphenols on Algae under Conditions of Changes in pH of the Environment. Hydrobiological Journal 2008; 44:37–44 [View Article]
     [Google Scholar]
  63. Uzilday B, Turkan I, Ozgur R, Sekmen AH. Strategies of ROS regulation and antioxidant defense during transition from C3 to C4 photosynthesis in the genus Flaveria under PEG-induced osmotic stress. J Plant Physiol 2014; 171:65–75 [View Article][PubMed]
     [Google Scholar]
  64. Mehterov N, Balazadeh S, Hille J, Toneva V, Mueller-Roeber B et al. Oxidative stress provokes distinct transcriptional responses in the stress-tolerant atr7 and stress-sensitive loh2 Arabidopsis thaliana mutants as revealed by multi-parallel quantitative real-time PCR analysis of ROS marker and antioxidant genes. Plant Physiol Biochem 2012; 59:20–29 [View Article][PubMed]
     [Google Scholar]
  65. Wrzaczek M, Brosché M, Kangasjärvi J. ROS signaling loops - production, perception, regulation. Curr Opin Plant Biol 2013; 16:575–582 [View Article][PubMed]
     [Google Scholar]
  66. Huang H, Xiao X, Lin F, Grossart HP, Nie Z et al. Continuous-release beads of natural allelochemicals for the long-term control of cyanobacterial growth: Preparation, release dynamics and inhibitory effects. Water Res 2016; 95:113–123 [View Article][PubMed]
     [Google Scholar]
  67. Ni L, Acharya K, Ren G, Li S, Li Y et al. Preparation and characterization of anti-algal sustained-release granules and their inhibitory effects on algae. Chemosphere 2013; 91:608–615 [View Article][PubMed]
     [Google Scholar]
  68. Viriyatum R. Effectiveness of coated controlled-released sulfate as an algicide for phytoplankton control in ponds. Fisheries & Allied Aquacultures 2013
     [Google Scholar]
  69. Viriyatum R, Boyd CE. Slow-release Coated Copper Sulfate as an Algicide for Aquaculture. J World Aquac Soc 2016; 47:667–675 [View Article]
     [Google Scholar]
  70. Touloupakis E, Margelou A, Ghanotakis DF. Intercalation of the herbicide atrazine in layered double hydroxides for controlled-release applications. Pest Manag Sci 2011; 67:837–841 [View Article][PubMed]
     [Google Scholar]
  71. Wen Y, Chen H, Yuan Y, Xu D, Kang X. Enantioselective ecotoxicity of the herbicide dichlorprop and complexes formed with chitosan in two fresh water green algae. J Environ Monit 2011; 13:879–885 [View Article][PubMed]
     [Google Scholar]
  72. Bae JH, Joo J-H, Lee YJ, Han M-S, Kim SH. Fabrication of biodegradable polylactide foam for algal bloom control. Fibers and Polymers 2015; 16:2087–2093 [View Article]
     [Google Scholar]
  73. Tian F, Zhou J, Sun Z, Cai Z, Xu N et al. Inhibitory effects of Chinese traditional herbs and herb-modified clays on the growth of harmful algae, Phaeocystis globosa and Prorocentrum donghaiense. Harmful Algae 2014; 37:153–159 [View Article]
     [Google Scholar]
  74. Guo P, Liu Y, Liu C. Effects of chitosan, gallic acid, and algicide on the physiological and biochemical properties of Microcystis flos-aquae. Environ Sci Pollut Res Int 2015; 22:13514–13521 [View Article][PubMed]
     [Google Scholar]
  75. Cheng S, Guo Y, Mao Y, Wang H, Yang Z et al. Inventors; Algaecide formulation used for preventing blue-green algae, comprises chitosan, autoclaved coal ash powder, and allelochemical containing gallic acid, azelaic acid, and N-phenyl-1-naphthylamine or N-phenyl-2-naphthylamine. China patent CN104671367-A; CN104671367-B2015-06-03–2016-08-10
     [Google Scholar]
  76. Lx N, Jie XT, Wang PF, Sy L, Wang GX et al. Effect of linoleic acid sustained-release microspheres on Microcystis aeruginosa antioxidant enzymes activity and microcystins production and release. Chemosphere 2015; 121:110–116
     [Google Scholar]
  77. Pan G, Chen J, Anderson DM. Modified local sands for the mitigation of harmful algal blooms. Harmful Algae 2011; 10:381–387 [View Article]
     [Google Scholar]
  78. Li L, Pan G. A universal method for flocculating harmful algal blooms in marine and fresh waters using modified sand. Environ Sci Technol 2013; 47:4555–4562 [View Article][PubMed]
     [Google Scholar]
  79. Pan G, Dai L, Li L, He L, Li H et al. Reducing the recruitment of sedimented algae and nutrient release into the overlying water using modified soil/sand flocculation-capping in eutrophic lakes. Environ Sci Technol 2012; 46:5077–5084 [View Article][PubMed]
     [Google Scholar]
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