Research Progresses and Application in the Growth-promoting Effect of Symbiotic and Epiphytic Bacteria on Green Tide-causing Ulva prolifera

doi:10.13560/j.cnki.biotech.bull.1985.2023-0652

Abstract

Abstract:

The migration and large-scale outbreak of green tides are not only related to the biological characteristics such as the strong stress resistance of algae and the environmental conditions of the sea area, but also inseparable from the participation of algal microorganisms. The microbial community plays an important role in algal growth and extinction. Under different environmental conditions, the community structure of symbiotic and epiphytic microorganisms of Ulva prolifera are diverse. The promotion to algae growth is mainly reflected in the processes of algae morphogenesis, growth, nutrient absorption and photosynthesis. During the occurrence of algal blooms, U. prolifera could help the algae to efficiently absorb nutrients, promote algae proliferation, and thus increase the formation of green tides. Based on previous researching results, we summarized the current research status of symbiotic and epiphytic bacteria of U. prolifera, the dominant species of green tide, described the establishment process of the separation technology of symbiotic and epiphytic bacteria of U. prolifera, and pointed out the importance of molecular biology techniques such as high-throughput sequencing in the analysis of microbial community structure and diversity, analyzed the influence of these bacteria on the physiological characteristics of the growth, reproduction, morphogenesis of U. prolifera and the outbreak of the green tides, and explored the utilization value of symbiotic and epiphytic bacteria in future production and life, aiming to express new ideas for predicting and preventing and controlling the outbreak of green tides and for the algal utilization as a resource.

Key words: green tide, Ulva prolifera, symbiotic and epiphytic bacterium, diversity, morphology, growth and development, propagation, stress resistance

BI Fang-ling, ZHAO Shuang, LI Bin, LI Ai-qin, ZHANG Jian-heng, HE Pei-min. Research Progresses and Application in the Growth-promoting Effect of Symbiotic and Epiphytic Bacteria on Green Tide-causing Ulva prolifera[J]. Biotechnology Bulletin, 2024, 40(1): 32-44.

Figures/Tables 2

References 108

[1]	Fraschetti S, Terlizzi A, Bevilacqua S, et al. The distribution of hydroids(Cnidaria, Hydrozoa)from micro- to macro-scale: spatial patterns on habitat-forming algae[J]. J Exp Mar Biol Ecol, 2006, 339(2): 148-158. doi: 10.1016/j.jembe.2006.07.007 URL
[2]	Schiel DR, Lilley SA. Gradients of disturbance to an algal canopy and the modification of an intertidal community[J]. Mar Ecol Prog Ser, 2007, 339: 1-11. doi: 10.3354/meps339001 URL
[3]	Zeng J, Yin BL, Wang YT, et al. Significantly decreasing harmful algal blooms in China Seas in the early 21st century[J]. Mar Pollut Bull, 2019, 139: 270-274. doi: S0025-326X(19)30002-5 pmid: 30686428
[4]	林森杰, 姬南京, 罗昊. 海洋有害藻华研究进展[J]. 海洋与湖沼, 2019, 50(3): 495-510.
	Lin SJ, Ji NJ, Luo H. Recent progress in marine harmful algal bloom research[J]. Oceanol Limnol Sin, 2019, 50(3): 495-510.
[5]	刘杰, 王晓姗, 王能飞, 等. 青岛近海浒苔粘附着细菌16S rDNA系统发育学研究[J]. 科学技术与工程, 2009, 9(8): 2042-2046, 2055.
	Liu J, Wang XS, Wang NF, et al. 16S rDNA phylogeny of adherent bacteria isolated from the surfaces of Enteromorpha prolifera in Qingdao Sea[J]. Sci Technol Eng, 2009, 9(8): 2042-2046, 2055.
[6]	施锦婷. 黄海绿潮浒苔种源的初步分析[D]. 上海: 上海海洋大学, 2019.
	Shi JT. Preliminary analysis of Ulva prolifera provenances in the Yellow Sea, China[D]. Shanghai: Shanghai Ocean University, 2019.
[7]	Fu ML, Cao SC, Li JS, et al. Controlling the main source of green tides in the Yellow Sea through the method of biological competition[J]. Mar Pollut Bull, 2022, 177: 113561. doi: 10.1016/j.marpolbul.2022.113561 URL
[8]	Huan L, Shi MM, Wang XL, et al. Morphological characteristics and genetic diversity of floating and attached Ulva prolifera - a case study in the Yellow Sea, China[J]. Mar Pollut Bull, 2023, 195: 115468. doi: 10.1016/j.marpolbul.2023.115468 URL
[9]	Chen ZH, Liu M, Yang YZ, et al. Environmental and economic impacts of different disposal options for Ulva prolifera green tide in the Yellow Sea, China[J]. ACS Sustainable Chem Eng, 2022, 10(35): 11483-11492. doi: 10.1021/acssuschemeng.2c02638 URL
[10]	Smetacek V, Zingone A. Green and golden seaweed tides on the rise[J]. Nature, 2013, 504(7478): 84-88. doi: 10.1038/nature12860
[11]	Zhang YY, He PM, Li HM, et al. Ulva prolifera green-tide outbreaks and their environmental impact in the Yellow Sea, China[J]. Natl Sci Rev, 2019, 6(4): 825-838. doi: 10.1093/nsr/nwz026 URL
[12]	唐晓雯, 范美华, 王超峰, 等. 外源CaCl₂调控浒苔(Ulva prolifera)高温逆境的比较转录组研究[J]. 海洋与湖沼, 2021, 52(3): 766-776.
	Tang XW, Fan MH, Wang CF, et al. Comparative transcriptome study of Ulva prolifera to calcium chloride treatment under high temperature stress[J]. Oceanol Limnol Sin, 2021, 52(3): 766-776.
[13]	Zhang XW, Wang HX, Mao YZ, et al. Somatic cells serve as a potential propagule bank of Enteromorpha prolifera forming a green tide in the Yellow Sea, China[J]. J Appl Phycol, 2010, 22(2): 173-180. doi: 10.1007/s10811-009-9437-6 URL
[14]	张健. 石莼属绿藻转录组测序及适应性进化机制研究[D]. 青岛: 青岛科技大学, 2021.
	Zhang J. Transcriptome sequencing and environmental adaptation analysis of Ulva[D]. Qingdao: Qingdao University of Science & Technology, 2021.
[15]	王广策, 唐学玺, 何培民, 等. 浒苔光合作用等关键生理过程对环境因子响应途径的研究进展[J]. 植物生理学报, 2016, 52(11): 1627-1636.
	Wang GC, Tang XX, He PM, et al. Progress of studies on the responses of the key physiological processes including photosynthese in Ulva prolifera O.F.Müller to environmental factors[J]. Plant Physiol J, 2016, 52(11): 1627-1636.
[16]	Liu Q, Yu RC, Yan T, et al. Laboratory study on the life history of bloom-forming Ulva prolifera in the Yellow Sea[J]. Estuar Coast Shelf Sci, 2015, 163: 82-88. doi: 10.1016/j.ecss.2014.08.011 URL
[17]	于仁成, 孙松, 颜天, 等. 黄海绿潮研究: 回顾与展望[J]. 海洋与湖沼, 2018, 49(5): 942-949.
	Yu RC, Sun S, Yan T, et al. Progresses and perspectives on green-tide studies in the Yellow Sea[J]. Oceanol Limnol Sin, 2018, 49(5): 942-949.
[18]	Jauzein C, Evans AN, Erdner DL. The impact of associated bacteria on morphology and physiology of the dinoflagellate Alexandrium tamarense[J]. Harmful Algae, 2015, 50: 65-75. doi: 10.1016/j.hal.2015.10.006 URL
[19]	Fu HH, Jiang P, Zhao J, et al. Comparative genomics of Pseudomonas sp. strain SI-3 associated with macroalga Ulva prolifera, the causative species for green tide in the Yellow Sea[J]. Front Microbiol, 2018, 9: 1458. doi: 10.3389/fmicb.2018.01458 URL
[20]	Qu TF, Hou CZ, Zhao XY, et al. Bacteria associated with Ulva prolifera: a vital role in green tide formation and migration[J]. Harmful Algae, 2021, 108: 102104. doi: 10.1016/j.hal.2021.102104 URL
[21]	Bell W, Mitchell R. Chemotactic and growth responses of marine bacteria to algal extracellular products[J]. Biol Bull, 1972, 143(2): 265-277. doi: 10.2307/1540052 URL
[22]	Yadav G, Meena M. Bioprospecting of endophytes in medicinal plants of Thar Desert: an attractive resource for biopharmaceuticals[J]. Biotechnol Rep, 2021, 30: e00629.
[23]	Singh RP, Reddy CRK. Seaweed-microbial interactions: key functions of seaweed-associated bacteria[J]. FEMS Microbiol Ecol, 2014, 88(2): 213-230. doi: 10.1111/1574-6941.12297 pmid: 24512602
[24]	Lasa AD, Auguste M, Lema A, et al. A deep-sea bacterium related to coastal marine pathogens[J]. Environ Microbiol, 2021, 23(9): 5349-5363. doi: 10.1111/1462-2920.15629 pmid: 34097814
[25]	Wichard T, Beemelmanns C. Role of chemical mediators in aquatic interactions across the prokaryote-eukaryote boundary[J]. J Chem Ecol, 2018, 44(11): 1008-1021. doi: 10.1007/s10886-018-1004-7 pmid: 30105643
[26]	包群靖, 毕芳玲, 蔡春尔, 等. 抗生素对浒苔形态及共附生细菌多样性的影响[J]. 海洋科学, 2023, 47(4): 108-116.
	Bao QJ, Bi FL, Cai CE, et al. Effects of antibiotics on the morphology and associated bacterial diversity of Ulva prolifera[J]. Mar Sci, 2023, 47(4): 108-116.
[27]	Blevins SM, Bronze MS. Robert Koch and the ‘golden age’ of bacteriology[J]. Int J Infect Dis, 2010, 14(9): e744-e751. doi: 10.1016/j.ijid.2009.12.003 URL
[28]	A guide to the identification of the Genera of bacteria[J]. J Clin Pathol, 1968, 21(2): 229-230.
[29]	孙创, 王金燕, 张钰琳, 等. 利用改良培养基探究西太平洋海水可培养细菌多样性[J]. 微生物学报, 2021, 61(4): 845-861.
	Sun C, Wang JY, Zhang YL, et al. Exploring the diversity of cultivated bacteria in the Western Pacific waters through improved culture media[J]. Acta Microbiol Sin, 2021, 61(4): 845-861.
[30]	陈騳, 林光恒, 沈世泽. 褐藻酸降解菌的研究——I.褐藻酸降解菌与褐藻酸酶对海带藻体的作用[J]. 海洋与湖沼, 1979, 10(4): 329-333, 402.
	Chen D, Lin GH, Shen SZ. Studies on alginic acid decomposing bacteria I. Action of alginic acid decomposing bacteria and alginase on laminaria japonica[J]. Oceanol Limnol Sin, 1979, 10(4): 329-333, 402.
[31]	武洪庆. 不同养殖海藻表面附着细菌多样性分析[D]. 青岛: 中国科学院研究生院(海洋研究所), 2012.
	Wu HQ. Epibacterial community structure of several macroalgae[D]. Qingdao: Institute of Oceanology, Chinese Academy of Sciences, 2012.
[32]	金柘. 绿潮浒苔共附生菌的多样性以及重要共附生菌影响其形态发育的研究[D]. 济南: 山东师范大学, 2018.
	Jin Z. Study on the diversity of the Ulva prolifera epiphytic bacteria in green tide and the effect of important co-bacteria on the morphological development[D]. Jinan: Shandong Normal University, 2018.
[33]	陈丽莹, 方荣祥, 吴建祥, 等. 植物内生细菌测定方法的研究进展[J]. 微生物学通报, 2022, 49(3): 1105-1119.
	Chen LY, Fang RX, Wu JX, et al. Research progress in the detection methods of endophytic bacteria[J]. Microbiol China, 2022, 49(3): 1105-1119.
[34]	Fisher MM, Wilcox LW, Graham LE. Molecular characterization of epiphytic bacterial communities on charophycean green algae[J]. Appl Environ Microbiol, 1998, 64(11): 4384-4389. doi: 10.1128/AEM.64.11.4384-4389.1998 URL
[35]	Kientz B, Thabard M, Cragg SM, et al. A new method for removing microflora from macroalgal surfaces: an important step for natural product discovery[J]. Botm, 2011, 54(5): 457-469. doi: 10.1515/BOT.2011.053 URL
[36]	陈冉. 浒苔附生菌的初步研究[D]. 上海: 上海海洋大学, 2018.
	Chen R. Preliminary study on epiphytic bacteria of Ulva prolifera[D]. Shanghai: Shanghai Ocean University, 2018.
[37]	Liu XJ, Zhao J, Jiang P. Easy removal of epiphytic bacteria on Ulva(Ulvophyceae, Chlorophyta)by Vortex with silica sands[J]. Microorganisms, 2022, 10(2): 476. doi: 10.3390/microorganisms10020476 URL
[38]	Alvarado P, Huang Y, Wang J, et al. Phylogeny and bioactivity of epiphytic Gram-positive bacteria isolated from three co-occurring Antarctic macroalgae[J]. Antonie Van Leeuwenhoek, 2018, 111(9): 1543-1555. doi: 10.1007/s10482-018-1044-6
[39]	Grueneberg J, Engelen AH, Costa R, et al. Macroalgal morphogenesis induced by waterborne compounds and bacteria in coastal seawater[J]. PLoS One, 2016, 11(1): e0146307. doi: 10.1371/journal.pone.0146307 URL
[40]	Zhao GH, He H, Wang HL, et al. Variations in marine bacterial and archaeal communities during an Ulva prolifera green tide in coastal Qingdao areas[J]. Microorganisms, 2022, 10(6): 1204. doi: 10.3390/microorganisms10061204 URL
[41]	苏秀榕, 秦松, 骆其君, 等. 浙江沿海藻类共生细菌的生理生化特性研究[J]. 生态环境, 2005, 14(2): 239-241.
	Su XR, Qin S, Luo QJ, et al. Physiology and biochemistry characteristic of symbiosis bacteria on algae of Zhejiang coast[J]. Ecol Environ Sci, 2005, 14(2): 239-241.
[42]	Tujula NA, Crocetti GR, Burke C, et al. Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga[J]. ISME J, 2010, 4(2): 301-311. doi: 10.1038/ismej.2009.107 pmid: 19829319
[43]	Nylund GM, Persson F, Lindegarth M, et al. The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence[J]. FEMS Microbiol Ecol, 2010, 71(1): 84-93. doi: 10.1111/j.1574-6941.2009.00791.x pmid: 19878319
[44]	Steen AD, Crits-Christoph A, Carini P, et al. High proportions of bacteria and Archaea across most biomes remain uncultured[J]. ISME J, 2019, 13(12): 3126-3130. doi: 10.1038/s41396-019-0484-y pmid: 31388130
[45]	邢磊, 赵圣国, 郑楠, 等. 未培养微生物分离培养技术研究进展[J]. 微生物学通报, 2017, 44(12): 3053-3066.
	Xing L, Zhao SG, Zheng N, et al. Advance in isolation and culture techniques of uncultured microbes: a review[J]. Microbiol China, 2017, 44(12): 3053-3066.
[46]	Tyson GW, Chapman J, Hugenholtz P, et al. Community structure and metabolism through reconstruction of microbial genomes from the environment[J]. Nature, 2004, 428(6978): 37-43. doi: 10.1038/nature02340
[47]	Li S, Lian WH, Han JR, et al. Capturing the microbial dark matter in desert soils using culturomics-based metagenomics and high-resolution analysis[J]. NPJ Biofilms Microbiomes, 2023, 9(1): 67. doi: 10.1038/s41522-023-00439-8
[48]	王宗灵, 傅明珠, 肖洁, 等. 黄海浒苔绿潮研究进展[J]. 海洋学报, 2018, 40(2): 1-13.
	Wang ZL, Fu MZ, Xiao J, et al. Progress on the study of the Yellow Sea green tides caused by Ulva prolifera[J]. Haiyang Xuebao, 2018, 40(2): 1-13.
[49]	Croft MT, Lawrence AD, Raux-Deery E, et al. Algae acquire vitamin B₁₂ through a symbiotic relationship with bacteria[J]. Nature, 2005, 438(7064): 90-93. doi: 10.1038/nature04056
[50]	Califano G, Kwantes M, Abreu MH, et al. Cultivating the macroalgal holobiont: effects of integrated multi-trophic aquaculture on the microbiome of Ulva rigida(Chlorophyta)[J]. Front Mar Sci, 2020, 7: 52. doi: 10.3389/fmars.2020.00052 URL
[51]	Wichard T. Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales(Chlorophyta)[J]. Front Plant Sci, 2015, 6: 86. doi: 10.3389/fpls.2015.00086 pmid: 25784916
[52]	Provasoli L, Pintner IJ. Bacteria induced polymorphism in an axenic laboratory strain of Ulva lactuca(Chlorophyceae)[J]. J Phycol, 1980, 16(2): 196-201. doi: 10.1111/jpy.1980.16.issue-2 URL
[53]	Matsuo Y, Suzuki M, Kasai H, et al. Isolation and phylogenetic characterization of bacteria capable of inducing differentiation in the green alga Monostroma oxyspermum[J]. Environ Microbiol, 2003, 5(1): 25-35. doi: 10.1046/j.1462-2920.2003.00382.x URL
[54]	吴春辉, 王峰, 赵瑾, 等. 浒苔原生质体再生苗对草丁膦与6种抗生素的敏感性[J]. 海洋科学, 2015, 39(8): 1-6.
	Wu CH, Wang F, Zhao J, et al. Sensitivity of protoplast-regenerated seedling of Ulva prolifera to phosphinothricin and six kinds of antibiotics[J]. Mar Sci, 2015, 39(8): 1-6.
[55]	Chen R, Cai C, Jiang T, et al. Growth and metagenomics analysis of Ulva prolifera after antibiotic treatment[J]. International Journal of Agriculture and Biology, 2019, 21(5): 1031-1035.
[56]	王瑜. 黄海绿潮浒苔生长发育的分子机理研究[D]. 济南: 山东大学, 2020.
	Wang Y. Molecular mechanism of growth and development of the green tides forming alga Ulva prolifera in the Yellow Sea[D]. Jinan: Shandong University, 2020.
[57]	Matsuo Y, Imagawa H, Nishizawa M, et al. Isolation of an algal morphogenesis inducer from a marine bacterium[J]. Science, 2005, 307(5715): 1598. pmid: 15761147
[58]	Marshall K, Joint I, Callow ME, et al. Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza[J]. Microb Ecol, 2006, 52(2): 302-310. pmid: 16897307
[59]	Berglund H. Stimulation of growth of two marine green algae by organic substances excreted by Enteromorpha linza in unialgal and axenic cultures[J]. Physiol Plant, 1969, 22(5): 1069-1073. doi: 10.1111/ppl.1969.22.issue-5 URL
[60]	Spoerner M, Wichard T, Bachhuber T, et al. Growth and thallus morphogenesis of Ulva mutabilis(Chlorophyta)depends on A combination of two bacterial species excreting regulatory factors[J]. J Phycol, 2012, 48(6): 1433-1447. doi: 10.1111/j.1529-8817.2012.01231.x pmid: 27009994
[61]	Alsufyani T, Weiss A, Wichard T. Time course exo-metabolomic profiling in the green marine macroalga Ulva(Chlorophyta)for identification of growth phase-dependent biomarkers[J]. Mar Drugs, 2017, 15(1): 14. doi: 10.3390/md15010014 URL
[62]	Wichard T. From model organism to application: bacteria-induced growth and development of the green seaweed Ulva and the potential of microbe leveraging in algal aquaculture[J]. Semin Cell Dev Biol, 2023, 134: 69-78. doi: 10.1016/j.semcdb.2022.04.007 URL
[63]	刘晓杰. 浒苔(Ulva prolifera)共附生细菌群落结构分析的方法学创新与CFB类群的初步研究[D]. 青岛: 中国科学院研究生院(海洋研究所), 2015.
	Liu XJ. Methodological innovation for analysis of the bacterial community structure and the study of CFB group associated with Ulva prolifera[D]. Qingdao: Institute of Oceanology, Chinese Academy of Sciences, 2015.
[64]	Ghaderiardakani F, Coates JC, Wichard T. Bacteria-induced morphogenesis of Ulva intestinalis and Ulva mutabilis(Chlorophyta): a contribution to the lottery theory[J]. FEMS Microbiol Ecol, 2017, 93(8): fix094.
[65]	Alsufyani T, Califano G, Deicke M, et al. Macroalgal-bacterial interactions: identification and role of thallusin in morphogenesis of the seaweed Ulva(Chlorophyta)[J]. J Exp Bot, 2020, 71(11): 3340-3349. doi: 10.1093/jxb/eraa066 pmid: 32016363
[66]	Hiraoka M, Ichihara K, Zhu WR, et al. Culture and hybridization experiments on an ulva clade including the Qingdao strain blooming in the Yellow Sea[J]. PLoS One, 2011, 6(5): e19371. doi: 10.1371/journal.pone.0019371 URL
[67]	Maruyama A, Maeda M, Simidu U. Distribution and classification of marine bacteria with the ability of cytokinin and auxin production[J]. Bull Jpn Soc Microb Ecol, 1990, 5(1): 1-8.
[68]	穆文强, 康慎敏, 李平兰. 根际促生菌对植物的生长促进作用及机制研究进展[J]. 生命科学, 2022, 34(2): 118-127.
	Mu WQ, Kang SM, Li PL. Advances in rhizosphere growth-promoting bacteria function on plant growth facilitation and their mechanisms[J]. Chin Bull Life Sci, 2022, 34(2): 118-127.
[69]	Zhao XY, Tang XX, Zhang HX, et al. Photosynthetic adaptation strategy of Ulva prolifera floating on the sea surface to environmental changes[J]. Plant Physiol Biochem, 2016, 107: 116-125. doi: 10.1016/j.plaphy.2016.05.036 URL
[70]	Shi XY, Qi MY, Tang HJ, et al. Spatial and temporal nutrient variations in the Yellow Sea and their effects on Ulva prolifera blooms[J]. Estuar Coast Shelf Sci, 2015, 163: 36-43. doi: 10.1016/j.ecss.2015.02.007 URL
[71]	Li HM, Zhang YY, Han XR, et al. Growth responses of Ulva prolifera to inorganic and organic nutrients: implications for macroalgal blooms in the southern Yellow Sea, China[J]. Sci Rep, 2016, 6: 26498. doi: 10.1038/srep26498
[72]	蒋雪蕾, 周晓见, 林佳宁, 等. 黄海浒苔绿潮生态效应研究进展[J]. 海洋环境科学, 2021, 40(4): 647-652.
	Jiang XL, Zhou XJ, Lin JN, et al. Research progress in the ecological consequences of Ulva prolifera green tides in the Yellow Sea[J]. Mar Environ Sci, 2021, 40(4): 647-652.
[73]	梅香远. 黄海金潮与绿潮致因种的共附生细菌群落结构与功能[D]. 青岛: 中国科学院大学(中国科学院海洋研究所), 2019.
	Mei XY. Community structures and functions of bacteria associated with blooming seaweeds in the Yellow Sea[D]. Qingdao: Institute of Oceanology, Chinese Academy of Sciences, 2019.
[74]	邹迪, 肖琳, 杨柳燕, 等. 不同形态磷源对铜绿微囊藻与附生假单胞菌磷代谢的影响[J]. 环境科学, 2005, 26(3): 118-121.
	Zou D, Xiao L, Yang LY, et al. Effects of phosphorus sources of different forms on phosphorus metabolism of Microcystis aeruginosa and adhesive Pseudomonas sp.[J]. Environ Sci, 2005, 26(3): 118-121. pmid: 16124482
[75]	Wang WL, Wu L, Xu K, et al. The cultivation of Pyropia haitanensis has important impacts on the seawater microbial community[J]. J Appl Phycol, 2020, 32(4): 2561-2573. doi: 10.1007/s10811-020-02068-6
[76]	Wahyudi A, Astuti R, Widyawati A, et al. Characterization of Bacillus sp. strains isolated from rhizosphere of soybean plants for their use as potential plant growth for promoting rhizobacteria[J]. J Microbiol Antimicrob, 2011, 3(2):34-40.
[77]	龚国利, 王亮, 王旭阳, 等. 植物内生芽孢杆菌的研究进展[J]. 生物学杂志, 2020, 37(3): 91-95.
	Gong GL, Wang L, Wang XY, et al. Research advances in plant endophytes Bacillaceae[J]. J Biol, 2020, 37(3): 91-95.
[78]	张亚茹, 张伟涛, 王硕, 等. 枯草芽孢杆菌N₂-10体外益生特性评价[J]. 饲料工业, 2020, 41(24): 12-17.
	Zhang YR, Zhang WT, Wang S, et al. Evaluation of in vitro probiotic properties of Bacillus subtilis N₂-10[J]. Feed Ind, 2020, 41(24): 12-17.
[79]	Crosbie DB, Mahmoudi M, Radl V, et al. Microbiome profiling reveals that Pseudomonas antagonises parasitic nodule colonisation of cheater rhizobia in Lotus[J]. New Phytol, 2022, 234(1): 242-255. doi: 10.1111/nph.17988 pmid: 35067935
[80]	李畅, 平文祥, 葛菁萍, 等. 微藻与其他微生物共培养的研究进展及应用[J]. 生物工程学报, 2022, 38(2): 518-530.
	Li C, Ping WX, Ge JP, et al. Advances in the co-culture of microalgae with other microorganisms and applications[J]. Chin J Biotechnol, 2022, 38(2): 518-530.
[81]	田川. 太湖浮游细菌分子生态学及溶藻细菌的研究[D]. 上海: 上海交通大学, 2012.
	Tian C. Research on bacterioplankton diversity and the algicidal bacteria in Lake Taihu[D]. Shanghai: Shanghai Jiao Tong University, 2012.
[82]	Kawano Y, Nagawa Y, Nakanishi H, et al. Production of thiotropocin by a marine bacterium, Caulobacter sp. and its antimicroalgal activities[J]. J Marine Biotechnology, 1997, 5: 225-229.
[83]	Yang F, Wei HY, Li XQ, et al. Isolation and characterization of an algicidal bacterium indigenous to Lake Taihu with a red pigment able to lyse microcystis aeruginosa[J]. Biomed Environ Sci, 2013, 26(2): 148-154. doi: 10.3967/0895-3988.2013.02.009 pmid: 23336138
[84]	Zhang X, Song T, Ma H, et al. Physiological response of Microcystis aeruginosa to the extracellular substances from an Aeromonas sp.[J]. RSC Adv, 2016, 6(105): 103662-103667. doi: 10.1039/C6RA17917G URL
[85]	陈莉婷, 左俊, 陶思依, 等. 利用微生物控制蓝藻研究进展[J]. 武汉大学学报: 理学版, 2019, 65(4): 401-410.
	Chen LT, Zuo J, Tao SY, et al. Progress in control of cyanobacteria by microorganism[J]. J Wuhan Univ Nat Sci Ed, 2019, 65(4): 401-410.
[86]	Imai I, Ishida Y, Hata Y. Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan[J]. Mar Biol, 1993, 116(4): 527-532. doi: 10.1007/BF00355470 URL
[87]	叶益华, 杨旭楠, 胡文哲, 等. 溶藻细菌的功能多样性及其菌剂应用[J]. 微生物学报, 2022, 62(4): 1171-1189.
	Ye YH, Yang XN, Hu WZ, et al. Advances in functional diversity and application of algicidal bacteria[J]. Acta Microbiol Sin, 2022, 62(4): 1171-1189.
[88]	Joint I, Callow ME, Callow JA, et al. The attachment of Enteromorpha zoospores to a bacterial biofilm assemblage[J]. Biofouling, 2000, 16(2/3/4): 151-158. doi: 10.1080/08927010009378440 URL
[89]	Patel P, Callow ME, Joint I, et al. Specificity in the settlement - modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha[J]. Environ Microbiol, 2003, 5(5): 338-349. doi: 10.1046/j.1462-2920.2003.00407.x URL
[90]	李孟珂, 夏运生, 单壮壮, 等. 三株蓝藻附着细菌多样性及其对铜绿微囊藻增殖的影响[J]. 云南大学学报: 自然科学版, 2019, 41(6): 1238-1245.
	Li MK, Xia YS, Shan ZZ, et al. Diversity of bacteria associated with three strains of cyanobacteria and their effects on the proliferation of Microcystis aeruginosa[J]. J Yunnan Univ Nat Sci Ed, 2019, 41(6): 1238-1245.
[91]	刘雅萌. 浒苔光合生理特性对海洋环境变化的响应[D]. 南京: 南京农业大学, 2014.
	Liu YM. The responses of photosynthetic physiological characteristics in Ulva species to the changes of marine environment[D]. Nanjing: Nanjing Agricultural University, 2014.
[92]	耿慧霞. 黄海绿潮原因种浒苔(Ulva prolifera)的附着生长特性与沉降区域研究[D]. 北京: 中国科学院大学, 2017.
	Geng HX. Study on the growth characteristics and subsidence area of Ulva prolifera, the cause of green tide in the Yellow Sea[D]. Beijing: University of Chinese Academy of Sciences, 2017.
[93]	周新倩, 杨锐, 吴小凯, 等. 基于16S rDNA分析的浒苔外生细菌多样性研究[J]. 水产学报, 2016, 40(1): 110-118.
	Zhou XQ, Yang R, Wu XK, et al. Diversity of Ulva spp.(Enteromorpha spp.) epiphytic bacteria based on 16S rDNA sequences[J]. J Fish China, 2016, 40(1): 110-118.
[94]	杨华田, 熊玉琴, 杨锐. 高温下芽孢杆菌对坛紫菜生长及生理的影响[J]. 水产学报, 2018, 42(7): 1009-1018.
	Yang HT, Xiong YQ, Yang R. Effects of Bacillus sp. on Pyropia haitanensis at high temperature[J]. J Fish China, 2018, 42(7): 1009-1018.
[95]	张忠山, 王晓梅, 刘峰, 等. 石莼属绿藻应答环境胁迫的生理特征与机制研究进展[J]. 海洋环境科学, 2020, 39(3): 473-479.
	Zhang ZS, Wang XM, Liu F, et al. Analysis of physiology and regulation mechanism of Ulva under stress[J]. Mar Environ Sci, 2020, 39(3): 473-479.
[96]	高珍. 浒苔生理生态特性和转录组研究[D]. 兰州: 甘肃农业大学, 2010.
	Gao Z. Study on physiological characteristics and the transcriptome of Enteromorpha prolifera[D]. Lanzhou: Gansu Agricultural University, 2010.
[97]	马茜, 王玉珏, 孙西艳, 等. 光和温度对两种绿潮藻光合途径及抗氧化功能的影响[J]. 海洋学报, 2020, 42(8): 21-29.
	Ma Q, Wang YJ, Sun XY, et al. Effects of light and temperature on the photosynthetic pathway and antioxidant function of two green tide species[J]. Haiyang Xuebao, 2020, 42(8): 21-29.
[98]	You ZZ, Zhang Q, Peng Z, et al. Lipid droplets mediate salt stress tolerance in Parachlorella kessleri[J]. Plant Physiol, 2019, 181(2): 510-526. doi: 10.1104/pp.19.00666 URL
[99]	周璇. 高盐胁迫下细菌—微藻的相互作用研究[D]. 武汉: 华中师范大学, 2017.
	Zhou X. Interaction between microalga and bacteria under high salt stress condition[D]. Wuhan: Central China Normal University, 2017.
[100]	邓凤飞, 杨双龙, 龚明. 细胞信号分子对非生物胁迫下植物脯氨酸代谢的调控[J]. 植物生理学报, 2015, 51(10): 1573-1582.
	Deng FF, Yang SL, Gong M. Regulation of cell signaling molecules on proline metabolism in plants under abiotic stress[J]. Plant Physiol J, 2015, 51(10): 1573-1582.
[101]	朱镕杰, 梅香远. 浒苔共附生菌——假交替单胞菌抗寒基因的筛选和应用[J]. 教育现代化, 2018, 5(44): 267-274.
	Zhu RJ, Mei XY. Screening and application of cold-resistant genes of Ulva prolifera symbiotic and epiphytic bacteria, Pseudoalteromonas sp.[J]. Educ Mod, 2018, 5(44): 267-274.
[102]	朱强, 夏艳秋, 顾冬莹, 等. 浒苔降解菌分离筛选与鉴定[J]. 安徽农业科学, 2017, 45(32): 152-155.
	Zhu Q, Xia YQ, Gu DY, et al. Isolation, screening and identification of Enteromorpha prolifera degrading bacterial strain[J]. J Anhui Agric Sci, 2017, 45(32): 152-155.
[103]	宋琳. 几种大型海藻硫酸多糖免疫相关活性及转录组学研究[D]. 青岛: 中国科学院大学(中国科学院海洋研究所), 2016.
	Song L. Immunomodulatory-related activity and RNA-seq research of six macroalgaes'sulfated polysaccharides[D]. Qingdao: Institute of Oceanology, Chinese Academy of Sciences, 2016.
[104]	李响, 周锡红, 赵玉蓉. 浒苔提取物成分分析及其生理功能研究进展[J]. 动物营养学报, 2019, 31(12): 5468-5475. doi: 10.3969/j.issn.1006-267x.2019.12.011
	Li X, Zhou XH, Zhao YR. Research progress on constitutes of Ulva prolifera extract and their biological function[J]. Chin J Anim Nutr, 2019, 31(12): 5468-5475.
[105]	顾铁基. 青岛潮间带沉积物细菌、浒苔多糖降解细菌的多样性分析及PL37家族浒苔多糖裂解酶的酶学性质研究[D]. 济南: 山东大学, 2021.
	Gu TJ. Diversity analysis of culturable bacteria in intertidal sediment of Qingdao and Enteromorpha prolifera polysaccharide degrading bacteria and the enzymatic properties of A PL37 family Enteromorpha prolifera polysaccharide lyase[D]. Jinan: Shandong University, 2021.
[106]	耿玉慧. 藻类附生菌多样性、多相分类鉴定及浒苔多糖降解酶的研究[D]. 济南: 山东大学, 2021.
	Geng YH. Studies on diversity and polyphasic identification of macroalgal epiphytic bacteria and Enteromorpha prolifera polysaccharide degrading enzymes[D]. Jinan: Shandong University, 2021.
[107]	Li YP, Li WH, Zhang GL, et al. Purification and characterization of polysaccharides degradases produced by Alteromonas sp. A321[J]. Int J Biol Macromol, 2016, 86: 96-104. doi: 10.1016/j.ijbiomac.2016.01.033 URL
[108]	苑志欣. 抗肿瘤浒苔共生微生物的筛选及其活性产物的研究[D]. 青岛: 青岛大学, 2018.
	Yuan ZX. Screening of anti-tumor symbiotic microorganisms of Enteromorpha prolifera and study on the active substance isolated from them[D]. Qingdao: Qingdao University, 2018.

物种Species	抗生素配方Antibiotic formulations	参考文献Reference
石莼U. lactuca	青霉素G、氯霉素、新霉素、硫酸多黏菌素B Penicillin G, chloramphenicol, neomycin, and polymyxin B sulfate	[52]
浒苔U. prolifera	青霉素G、硫酸新霉素、多黏菌素B Penicillin G, neomycin sulfate, and polymyxin B 青霉素G、氯霉素、诺氟沙星、链霉素、卡那霉素 Penicillin G, chloramphenicol, norfloxacin, streptomycin, and kanamycin	[32,55-56]
孔石莼U. pertusa	青霉素G、链霉素、红霉素、卡那霉素Penicillin G, streptomycin, erythromycin, and kanamycin	[57]
缘管浒苔U. linza	青霉素G、链霉素、诺氟沙星、卡那霉素 Penicillin G, streptomycin, norfloxacin, and kanamycin	[58]
缘管浒苔Enteromorpha linza	青霉素、链霉素Penicillin and streptomycin	[59]

物种Species	抗生素配方Antibiotic formulations	参考文献Reference
石莼U. lactuca	青霉素G、氯霉素、新霉素、硫酸多黏菌素B Penicillin G, chloramphenicol, neomycin, and polymyxin B sulfate	[52]
浒苔U. prolifera	青霉素G、硫酸新霉素、多黏菌素B Penicillin G, neomycin sulfate, and polymyxin B 青霉素G、氯霉素、诺氟沙星、链霉素、卡那霉素 Penicillin G, chloramphenicol, norfloxacin, streptomycin, and kanamycin	[32,55-56]
孔石莼U. pertusa	青霉素G、链霉素、红霉素、卡那霉素Penicillin G, streptomycin, erythromycin, and kanamycin	[57]
缘管浒苔U. linza	青霉素G、链霉素、诺氟沙星、卡那霉素 Penicillin G, streptomycin, norfloxacin, and kanamycin	[58]
缘管浒苔Enteromorpha linza	青霉素、链霉素Penicillin and streptomycin	[59]