Terpenoid-induced algal inhibition and the co-culture of terpene-enriched plants for algal suppression
JIANG Yu-meng1, ZHANG Wen-le1, LUO Zhao-hui1, LI Hui-xin1, CHEN Dan2
1. College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210014, China; 2. College of Agricultural Science and Engineering, Hohai University, Nanjing 210013, China
Abstract：In order to solve the problem of cyanobacteria bloom in freshwater bodies in summer, Microcystis aeruginosa was taken as the research object, and six terpenoid compounds including menthol, borneol, geraniol, andrographolide, linalool and citral were selected to screen high-efficiency algaecides, and their algaecological effects, mechanisms, application methods and ecological safety were explored. The results showed that geraniol and citral had the best inhibitory effects on Microcystis aeruginosa, and the inhibition rate increased with the increase of concentration. At a concentration of 60mg/L, The maximum inhibition rates of geraniol and citral were 86.9% and 76.0%, respectively. Under the action of geraniol and citral, the chlorophyll a and carotenoid contents of Microcystis aeruginosa decreased, photosynthesis was inhibited; the activity of antioxidant enzymes decreased, and reactive oxygen accumulated in cells; free radicals attacked the cell membrane, and the cell structure was damaged, leading to the death of algal cells. Geraniol and citral did not have the properties of "low promotion and high inhibition". They were less toxic to Chlamydomonas and Brachionus calyciflorus, and had no significant effect on Elodea and Zebrafish, and had a certain ecological safety. Geraniol-rich Melissa officinalis and citral-rich Citronella showed significant algal inhibition in co-culture with Microcystis aeruginosa with algal inhibition rate as high as 95%, which is suitable to be used as floating-bed plants for the prevention and control of cyanobacterial blooms.
[1] 许明,刘伟京,白永刚,等.太湖蓝藻水华期可溶有机物的生物降解[J]. 中国环境科学, 2018,38(9):3494-3501. Xu M, Liu W J, Bai Y G, et al. Biodegradation of soluble organic matter during cyanobacteria bloom in Taihu Lake [J]. Chinese Environmental Science, 2018,38(9):3494-3501. [2] 李加龙,罗纯良,吕恒,等.2002~2018年滇池外海蓝藻水华暴发时空变化特征及其驱动因子[J]. 生态学报, 2023,43(2):878-891. Li J L, Luo C L, Lu H, et al. Temporal and spatial variations of cyanobacteria bloom outbreaks in Dianchi Lake from 2002 to 2018 and their driving factors [J]. Acta Ecologica Sinica, 2023,43(2):878- 891. [3] 胡旻琪,张玉超,马荣华,等.巢湖2016年蓝藻水华时空分布及环境驱动力分析[J]. 环境科学, 2018,39(11):4925-4937. Hu M Q, Zhang Y C, Ma R H, et al. Spatial and temporal distribution and environmental driving forces of cyanobacteria blooms in Chaohu Lake in 2016[J]. Environmental Science, 2018,39(11):4925-4937. [4] Plaas H E, Paerl H W. Toxic Cyanobacteria: A growing threat to water and air quality [J]. Environmental Science & Technology, 2021,55(1): 44-64. [5] 史小丽,杨瑾晟,陈开宁,等.湖泊蓝藻水华防控方法综述[J]. 湖泊科学, 2022,34(2):349-375. Shi X L, Yang J S, Chen K N, et al. Review on control methods of cyanobacteria bloom in lakes [J]. Lake Science, 2022,34(2):349-75. [6] Fan F, Shi X, Zhang M, et al. Comparison of algal harvest and hydrogen peroxide treatment in mitigating cyanobacterial blooms via an in situ mesocosm experiment [J]. Science of the Total Environment, 2019,694(2019):133721. [7] 陈贺林,李芸,储昭升,等.超声波控藻技术现状及研究进展[J]. 环境工程技术学报, 2020,10(1):72-78. Chen H L, Li Y, Chun Z S, et al. Current status and research progress of ultrasonic algal control technology [J]. Journal of Environmental Engineering Technology, 2020,10(1):72-78. [8] 杨瑾晟,姜磊,芦津,等.絮凝控制高浓度藻华对水质和植被恢复的影响[J]. 中国环境科学, 2023,43(2):561-567. Yang J S, Jiang L, Lu J, et al. Effects of flocculation control on high concentration algal blooms on water quality and vegetation restoration [J]. Chinese Environmental Science, 2023,43(2):561-567. [9] Lurling M, Mucci M. Mitigating eutrophication nuisance: in-lake measures are becoming inevitable in eutrophic waters in the Netherlands [J]. Hydrobiologia, 2020,847(21):4447-4467. [10] 王敏,刘浩,王江南,等.生物法治理蓝藻水华研究进展[J]. 环境工程技术学报, 2022,12(1):92-99. Wang M, Liu H, Wang J N, et al. Research progress on biological control of cyanobacteria bloom [J]. Journal of Environmental Engineering Technology, 2022,12(1):92-99. [11] 王巍,刘吉祥,孙林鹤,等.浮床水芹不同器官酚酸类和脂肪酸类化感物质代谢组学分析[J]. 浙江农业学报, 2023,35(11):2673-2687. Wang W, Liu J X, Sun H L, et al. Metabolomics analysis of phenolic acids and fatty acids allelopathic substances in different organs of watercress [J]. Zhejiang Agricultural journal, 2023,35(11):2673-2687. [12] 陈晶莹,周炜杰,林果,等.沉水态圆叶节节菜的化感抑藻作用[J]. 浙江农林大学学报, 2023,40(4):765-772. Chen J Y, Zhou W J, Lin G, et al. Allelopathy and algal inhibition of submerged round leaf vegetable [J]. Journal of Zhejiang A & F University, 2023,40(4):765-772. [13] Nakai S, Inoue Y, Hosomi M, et al. Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa [J]. Water Research, 2000,34(11):3026-3032. [14] He Y, Zhou Q H, Liu B Y, et al. Programmed cell death in the cyanobacterium Microcystis aeruginosa induced by allelopathic effect of submerged macrophyte Myriophyllum spicatum in co-culture system [J]. Journal of Applied Phycology, 2016,28(5):2805-2814. [15] Ni L, Zhu C, Du C, et al. Characterization of a novel artemisinin algicidal particle and its inhibitory effect on microcystis aeruginosa [J]. Bulletin of Environmental Contamination and Toxicology, 2023,110(5):82. [16] 姚远,贺锋,胡胜华,等.沉水植物化感作用对西湖湿地浮游植物群落的影响[J]. 生态学报, 2016,36(4):971-978. Yao Y, He F, Hu S H, et al. Effects of allelopathy of submerged plants on phytoplankton community in West Lake wetland [J]. Acta Ecologica Sinica, 2016,36(4):971-978. [17] 蒋跃.浮床植物生态特性及其抑藻效果研究[D]. 上海:华东师范大学, 2016. Jiang Y. Study on ecological characteristics of floating bed plants and their effect on inhibiting algae [D]. Shanghai: East China Normal University, 2016. [18] 赵倩名,钟佳峻,何培民,等.黄酮类物质对铜绿微囊藻的抑制效应研究[J]. 环境科学与技术, 2022,45(2):1-7. Zhao Q M, Zhong J J, He P M, et al. Inhibitory effect of flavonoids on Microcystis aeruginosa [J]. Environmental Science and technology, 2022,45(2):1-7. [19] 侯新星,田如男.有机酸对铜绿微囊藻生长及光合色素的影响[J]. 生物学杂志, 2021,38(4):65-70. Hou X X, Tian R N. Effects of organic acids on the growth and photosynthetic pigments of microcystis aeruginosa [J]. Journal of biology, 2021,38(4):65-70. [20] 杨超慧,王超,欧阳萍,等.丙二酸对铜绿微囊藻的抑制效果[J]. 水资源保护, 2021,37(3):121-126. Yang C H, Wang C, Ouyang P, et al. Inhibitory effect of malonic acid on microcystis aeruginosa [J]. Water Resources Protection, 2021,37(3): 121-126. [21] 朱小琴,刀国华,陶益,等.典型植物化感物质对铜绿微囊藻生长的抑制效果评价[J]. 中国环境科学, 2020,40(5):2230-2237. Zhu X Q, Dao G H, Tao Y, et al. Evaluation of inhibitory effect of typical plant allelochemicals on Microcystis aeruginosa [J]. Chinese Environmental Science, 2020,40(5):2230-2237. [22] 李德全,胡杰,罗俊容,等.薄荷醇杀菌效果的初步研究[J]. 中国消毒学杂志, 2022,39(5):334-336. Li D Q, Hu J, Luo J R, et al. Preliminary study on bactericidal effect of menthol [J]. Chinese Journal of Disinfection, 2022,39(5):334-336. [23] 刘文杰,张晓寒,吴佳欢,等.井冈山地区龙脑樟来源真菌多样性和抗菌活性研究[J]. 中国抗生素杂志, 2022,47(7):631-637. Liu W J, Zhang X H, Wu J H, et al. Study on diversity and antibacterial activity of camphor derived fungi in Jinggangshan area [J]. Chinese Journal of Antibiotics, 2022,47(7):631-637. [24] 翁甜,王昱晴,龙超安.香叶醇对柑橘酸腐病菌的抑菌机制[J]. 食品科学, 2023,44(1):14-21. Weng T, Wang Y Q, Long C A. Bacteriostatic mechanism of geraniol against citrus sour rot bacteria [J]. Food Science, 2023,44(1):14-21. [25] Tang T, Zhong W, Yang L, et al. In vitro and in vivo anti-oomycetes activities and mechanisms of linalool against Saprolegnia ferax [J]. Aquaculture, 2024,578:740031. [26] Yigui Q, Zihui Y, Xuebao S, et al. Synthesis and antifungal activity of novel L-Menthol hydrazide derivatives as potential laccase inhibitors [J]. Chemistry & biodiversity, 2023,20(7):e202300539. [27] 胡珊,梁卫驱,黄皓,等.不同化学型樟树精油的化学成分和抑菌效果研究[J]. 安徽农业科学, 2022,50(22):193-197. Hu S, Liang W Q, Huang H, et al. Study on chemical constituents and antibacterial effects of different chemical types of camphor essential oils [J]. Anhui Agricultural Sciences, 2022,50(22):193-197. [28] 母育成,邢相宜,晏子俊,等.穿心莲内酯的抗菌作用研究进展[J]. 贵州中医药大学学报, 2021,43(1):85-89. Mu Y C, Xing X Y, Yan Z J, et al. Research progress on the antibacterial effect of andrographolide [J]. Journal of Guizhou University of Chinese Medicine, 2021,43(1):85-89. [29] Wen J, Liao H, Nie H, et al. Comprehensive transcriptomics and metabolomics revealed the antifungal mechanism of Cymbopogon citratus essential oil nanoemulsion against Fusarium solani [J]. Chemical and Biological Technologies in Agriculture, 2023,10(1):142. [30] 郭峰,董明辉,高梦园,等.柠檬香蜂草精油的气相色谱-质谱联用分析及抑菌活性研究[J]. 食品与发酵工业, 2021,47(2):109-113. Guo F, Dong M H, Gao M Y, et al. Analysis and antibacterial activity of lemon balm essential oil by gas chromatography-mass spectrometry [J]. Food and Fermentation industry, 2021,47(2):109-113. [31] 赵红艳,王娇,曹井国,等.芦荟大黄素对铜绿微囊藻的化感抑制作用研究[J]. 生物学杂志, 2020,37(5):53-57. Zhao H Y, Wang J, Cao J G, et al. Allelopathic inhibition of aloe emodin on Microcystis aeruginosa [J]. Journal of Biology, 2020,37(5):53-57. [32] Lichtenthaler H K, Wellburn A R.Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents [J]. Analysis, 1983,11(5):591-592. [33] 苍晶,赵会杰.植物生理学实验教程[M]. 高等教育出版社, 2013. Cang J, Zhao H J. Experimental course in plant physiology [M]. Higher Education Press, 2013. [34] 严衍禄,刘心生.叶绿素测定方法的研究[J]. 北京农业大学学报, 1982,8(2):53-67. Yan Y L, Liu X S. Study on the determination method of chlorophyll [J]. Journal of Beijing Agricultural University, 1982,8(2):53-67. [35] 祝志林.两种观赏型水生植物对铜绿微囊藻生长的抑制作用研究[D]. 长沙:湖南大学, 2014. Zhu Z L. Inhibitory effects of two ornamental aquatic plants on the growth of Microcystis aeruginosa [D]. Changsha: Hunan University, 2014. [36] 周伟.基于化感作用的新型抑藻剂筛选及其生态安全性初探[D]. 上海:上海海洋大学, 2020. Zhou W. Screening and ecological safety of novel algal suppressants based on allelopathy [D]. Shanghai: Shanghai Ocean University, 2020. [37] Suzuki Y, Saijo H, Takahashi K, et al. Growth-inhibitory components in Sugi (Cryptomeria japonica) extracts active against Microcystis aeruginosa [J]. Cogent Environmental Science, 2018,4(1):1466401. [38] Ni L X, Hao X Y, Li S Y, et al. Inhibitory effects of the extracts with different solvents from three compositae plants on cyanobacterium Microcystis aeruginosas [J]. Science China Chemistry, 2011,54(7): 1123-1129. [39] 徐芙清,何伟,郑星,等.野艾蒿及其有机提取物对铜绿微囊藻生长的抑制作用[J]. 生态学报, 2010,30(3):745-750. Xu F Q, He W, Zheng X, et al. Inhibition of Artemisia Argus and its organic extracts on the growth of Microcystis aeruginosa [J]. Acta Ecologica Sinica, 2010,30(3):745-750. [40] Hu X, Liu Y, Zeng G, et al. Effects of limonene stress on the growth of and microcystin release by the freshwater cyanobacterium Microcystis aeruginosa FACHB-905[J]. Ecotoxicology and Environmental Safety, 2014,105:121-127. [41] Hu X, Liu Y, Zeng G, et al. Effects of D-menthol stress on the growth of and microcystin release by the freshwater cyanobacterium Microcystis aeruginosa FACHB-905[J]. Chemosphere, 2014,113:30- 35. [42] 甘小蓉,王超,杨超慧.4种化感物质对铜绿微囊藻生长及叶绿素荧光参数影响的比较[J]. 四川环境, 2019,38(5):1-6. Gan X R, Wang C, Yang C H. Comparison of the effects of four allelochemicals on the growth and chlorophyll fluorescence parameters of Microcystis aeruginosa [J]. Environment of Sichuan, 2019,3805:1-6. [43] Guo Z-H, Li J-M, Zhang M-X. A review on antialgal effectiveness among distinct allelochemicals and joint inhibitory effects on cyanobacterial growth [J]. Acta Hydrobiologica Sinica, 2023,47(1): 177-194. [44] Ni L, Jie X, Wang P, et al. Effect of linoleic acid sustained-release microspheres on Microcystis aeruginosa antioxidant enzymes activity and microcystins production and release [J]. Chemosphere, 2015, 121:110-116. [45] Paerl H W, Bland P T, Bowles N D, et al. Adaptation to high-Intensity, low-wavelength light among surface blooms of the cyanobacterium microcystis aeruginosa [J]. Applied and Environmental Microbiology, 1985,49(5):1046-1052. [46] Wang Y S, Tian S P, Xu Y, et al. Changes in the activities of pro- and anti-oxidant enzymes in peach fruit inoculated with Cryptococcus laurentii or Penicillium expansum at 0 or 20℃ [J]. Postharvest Biology and Technology, 2004,34(1):21-28. [47] Mallick N, Mohn F H. Reactive oxygen species: response of algal cells [J]. Journal of Plant Physiology, 2000,157(2):183-193. [48] Ni L X, Li X L, Xu C, et al. Stress of artemisinin sustained-release granules on photosystem II, reactive oxygen species and metabolic activity of microcystis aeruginosa cells [J]. Bulletin of Environmental Contamination and Toxicology, 2021,107(2):343-350. [49] 段元静,钟晓婷,陈超志,等.柠檬草与香茅药材中柠檬醛、香叶醇的定性定量研究[J]. 广东药学院学报, 2016,32(6):690-694. Duan Y J, Zhong X T, Chen C Z, et al. Qualitative and quantitative study on citral and geraniol in lemongrass and citronella [J]. Journal of Guangdong Pharmaceutical University, 2016,32(6):690-694. [50] 李明军.植物与植物生理[M]. 重庆:重庆大学出版社, 2015. Li M J . Plants and plant physiology [M]. Chongqing: Chongqing University Press, 2015.
