The research progress of microorganisms in seagrass meadows
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摘要: 海草是一类生长于海洋环境中的单子叶植物。细菌、真菌、微藻、古生菌和病毒等微生物栖息在海草器官及其周围环境中,对海草生长、营养和健康以及海草床物质循环起着重要作用。本文通过分析与总结国内外参考文献,简要介绍了海草床微生物的一些新的研究进展,并讨论了将来可能进行的研究方向。海草微生物组与沉积物和海水中的微生物群落存在较大差异,其分布在离散且高度异质性的生态位,且该模式在广泛的地理尺度上保持不变,不是受海草种类和沉积物类型控制,而是主要取决于环境驱动与海草代谢。大部分海草核心微生物群落都参与硫循环。今后可采用模拟实验、生态模型、基因组、宏基因组、转录组与代谢组等技术方法研究海草床微生物的多样性、组成、功能、定植与病害等。此外,揭示海草床中微生物、海草和环境之间的相互关系,对保护受威胁的海草床具有重要意义。Abstract: Seagrass are a kind of monocotyledonous plants growing in marine environments. Microorganisms such as bacteria, fungi, microalgae, archaea and viruses inhabiting seagrass organs and environment play an important role in controlling growth, nutrition and health of seagrass, and maintaining material cycling in seagrass meadows. In this paper, we briefly summarized some recent progresses in studying of microorganisms in seagrass meadows, and discussed the possible directions for future research in this area. Seagrasses microbiome is significantly different from the microbial community in sediment and seawater, which is distributed in discrete and highly heterogeneous ecological niches, and the model remains consistent on a wide geographical scale. It is not controlled by the seagrasses species and sediment types, but mainly depended on the environment and the metabolism of seagrasses. Most seagrass core microbial communities are associated with the sulfur cycle. In the future, methods such as simulation experiment, the ecological model, genome, metagenome, metatranscriptome and metabolome can be used to study diversity, composition, function, colonization and diseases of microorganisms in seagrass meadows. Additionally, it is of great significance to reveal the interrelationships among microorganisms, seagrasses and the environment for the protection of threatened seagrass meadows.
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Key words:
- seagrass meadows /
- holobiont /
- core microbiome /
- diversity /
- environment
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表 1 已知的海草病原体和宿主
Tab. 1 Known seagrass pathogens and hosts
海草宿主 病原体 症状 参考文献 Zostera marina Oomycetes, Heterokonta 抑制和降低海草种子萌发,抑制
幼苗发育[47−48] Zostera marina, Zostera muelleri, Zostera caulescens,
Zostera japonica, Zostera noltii, Zostera pacifica, Cymodocea nodosa, Posidonia oceanica
Ruppia cirrhosa, Ruppia maritima, Syringodium isoetifolium, Thalassia testudinum,Labyrinthulomycetes,Heterokonta 海草叶子损伤 [51] Halophila ovalis Phytomyxea, Rhizaria, Plasmodiophora 枝瘿 [45] Ruppia brachypus, Ruppia rostellata, Ruppia spiralis, Ruppia maritimus Phytomyxea, Rhizaria 枝瘿 [45] -
[1] 杨宗岱. 中国海草植物地理学的研究[J]. 海洋湖沼通报, 1979(2): 41−46.Yang Zongdai. The geographical distribution of sea-grasses[J]. Transactions of Oceanology and Limnology, 1979(2): 41−46. [2] William C D, Robert J O, Kenneth A M, et al. Assessing water quality with submersed aquatic vegetation[J]. BioScience, 1993, 43(2): 86−94. doi: 10.2307/1311969 [3] 黄小平, 黄良民, 李颖虹, 等. 华南沿海主要海草床及其生境威胁[J]. 科学通报, 2006, 51(S2): 136−142. doi: 10.1007/s11434-006-9136-5Huang Xiaoping, Huang Liangmin, Li Yinghong, et al. Main seagrass beds and threats to their habitats in the coastal sea of South China[J]. Chinese Science Bulletin, 2006, 51(S2): 136−142. doi: 10.1007/s11434-006-9136-5 [4] Orth R J, Carruthers T J B, Dennison W C, et al. A global crisis for seagrass ecosystems[J]. BioScience, 2006, 56(12): 987−996. doi: 10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2 [5] De Iongh H H, Kiswara W, Kustiawan W, et al. A review of research on the interactions between dugongs (Dugong dugon Müller 1776) and intertidal seagrass beds in Indonesia[J]. Hydrobiology, 2007, 591(1): 73−83. doi: 10.1007/s10750-007-0785-4 [6] Duarte C M, Borum J, Short F T, et al. Seagrass Ecosystems: Their Global Status and Prospects[M]. London: Cambridge University Press, 2008: 38−125. [7] 李文涛, 张秀梅. 海草场的生态功能[J]. 中国海洋大学学报, 2009, 39(5): 933−939.Li Wentao, Zhang Xiumei. The ecological functions of seagrass meadows[J]. Periodical of Ocean University of China, 2009, 39(5): 933−939. [8] 王锁民, 崔彦农, 刘金祥, 等. 海草及海草场生态系统研究进展[J]. 草业学报, 2016, 25(11): 149−159. doi: 10.11686/cyxb2016025Wang Suomin, Cui Yannong, Liu Jinxiang, et al. Research progress on seagrass and seagrass ecosystems[J]. Acta Prataculturae Sinica, 2016, 25(11): 149−159. doi: 10.11686/cyxb2016025 [9] Waycott M, Duarte C M, Carruthers T J, et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems[J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(30): 12377−12381. doi: 10.1073/pnas.0905620106 [10] Lee K S, Dunton K H. Production and carbon reserve dynamics of the seagrass Thalassia testudinum in Corpus Christi Bay, Texas, USA[J]. Marine Ecology Progress Series, 1996, 43(1/3): 201−210. [11] 郑凤英, 邱广龙, 范航清, 等. 中国海草的多样性、分布及保护[J]. 生物多样性, 2013, 21(5): 517−526.Zheng Fengying, Qiu Guanglong, Fan Hangqing, et al. Diversity, distribution and conservation of Chinese seagrass species[J]. Biodiversity Science, 2013, 21(5): 517−526. [12] Short F T, Polidoro B, Livingstone S R, et al. Extinction risk assessment of the world’s seagrass species[J]. Biological Conservation, 2011, 144(7): 1961−1971. doi: 10.1016/j.biocon.2011.04.010 [13] Larkum A W D, Orth R J, Duarte C M. Seagrasses: Biology, Ecology and Conservation[M]. Netherlands: Springer, 2006: 6−91. [14] 王道儒, 吴钟解, 陈春华, 等. 海南岛海草资源分布现状及存在威胁[J]. 海洋环境科学, 2012, 31(1): 34−38. doi: 10.3969/j.issn.1007-6336.2012.01.008Wang Daoru, Wu Zhongjie, Chen Chunhua, et al. Distribution of sea-grass resources and existing threat in Hainan Island[J]. Marine Environmental Science, 2012, 31(1): 34−38. doi: 10.3969/j.issn.1007-6336.2012.01.008 [15] 范航清, 石雅君, 邱广龙. 中国海草植物[M]. 北京: 海洋出版社, 2009: 1-55.Fang Hangqing, Shi Yajun, Qiu Guanglong. China Seagrass Plants[M]. Beijing: China Ocean Press, 2009: 1−55. [16] Short F, Carruthers T, Dennison W, et al. Global seagrass distribution and diversity: a bioregional model[J]. Journal of Experimental Marine Biology and Ecology, 2007, 350(1/2): 3−20. [17] Unsworth R K F, McKenzie L J, Collier C J, et al. Global challenges for seagrass conservation[J]. Ambio, 2019, 48(8): 801−815. doi: 10.1007/s13280-018-1115-y [18] 黄小平, 江志坚, 张景平, 等. 全球海草的中文命名[J]. 海洋学报, 2018, 40(4): 127−133.Huang Xiaoping, Jiang Zhijian, Zhang Jingping, et al. The Chinese nomenclature of the global seagrasses[J]. Haiyang Xuebao, 2018, 40(4): 127−133. [19] 黄小平, 江志坚, 范航清, 等. 中国海草的“藻”名更改[J]. 海洋与湖沼, 2016, 47(1): 290−294.Huang Xiaoping, Jiang Zhijian, Fang Hangqing, et al. The nomenclature of the "algae" name of seagrasses in China[J]. Oceanologia et Limnologia Sinica, 2016, 47(1): 290−294. [20] Charpy R C, Sournia A. The comparative estimation of phytoplanktonic, microphytobenthic and macrophytobentic primary production in the oceans[J]. Marine Microbial Food Webs, 1990, 4(1): 31−57. [21] Fourqurean J W, Johnson B J, Kauffman J B, et al. Field sampling of vegetative carbon pools in coastal ecosystems[M]//Howard J, Hoyt S, Isesnsee K, et al. Conservation International, Intergovernmental Oceanographic Commission of UNESCO. Arlington: International Union for Conservation of Nature, 2014: 67−108. [22] 韩秋影. 海草床衰退机制及管理[M]. 北京: 科学出版社, 2016: 1−17Han Qiuying. Decline Mechanism and Management of Seagrass Beds[M]. Beijing: Science Press, 2016: 1−17. [23] Nielsen L W, Dahllof I. Direct and indirect effects of the herbicides glyphosate, bentazone and MCPA on eelgrass (Zostera marina)[J]. Aquatic Toxicology, 2007, 82(1): 47−54. doi: 10.1016/j.aquatox.2007.01.004 [24] Lamb J B, Van De Water J A J M, Bourne D G, et al. Seagrass ecosystems reduce exposure to bacterial pathogens of humans, fishes, and invertebrates[J]. Science, 2017, 355(6326): 731−733. doi: 10.1126/science.aal1956 [25] 江玉凤. 南海新村湾海草床生态系统微生物群落结构、分布及固氮微生物多样性研究[D]. 广州: 中国科学院南海海洋研究所, 2016.Jiang Yufeng. Study on microbial community structure, distribution and diazotrophic diversity in seagrass meadow, Xincun Bay, South China Sea[D]. Guangzhou: South China Sea Institute of Oceanology, Chinese Academy of Sciences, 2016. [26] Gullström M, De La Torre Castro M, Bandeira S O, et al. Seagrass ecosystems in the Western Indian Ocean[J]. Ambio, 2002, 31(7): 588−596. doi: 10.1579/0044-7447-31.7.588 [27] Bertelli C M, Unsworth R K F. Protecting the hand that feeds us: seagrass (Zostera marina) serves as commercial juvenile fish habitat[J]. Marine Pollution Bulletin, 2014, 83(2): 425−429. doi: 10.1016/j.marpolbul.2013.08.011 [28] Guannel G, Arkema K, Ruggiero P, et al. The power of three: coral reefs, seagrasses and mangroves protect coastal regions and increase their resilience[J]. PloS One, 2016, 11(7): e0158094. doi: 10.1371/journal.pone.0158094 [29] Herbeck L S, Sollich M, Unger D, et al. Impact of pond aquaculture effluents on seagrass performance in NE Hainan, tropical China[J]. Marine Pollution Bulletin, 2014, 85(1): 190−203. doi: 10.1016/j.marpolbul.2014.05.050 [30] Burkholder J M, Tomasko D A, Touchette B W. Seagrasses and eutrophication[J]. Journal of Experimental Marine Biology and Ecology, 2007, 350(1/2): 46−72. [31] Fertig B, Kennish M J, Sakowicz G P. Changing eelgrass (Zostera marina L.) characteristics in a highly eutrophic temperate coastal lagoon[J]. Aquatic Botany, 2013, 104: 70−79. doi: 10.1016/j.aquabot.2012.09.004 [32] Silberstein K, Chiffings A W, McComb A J. The loss of seagrass in cockburn sound, Western Australia. III. The effect of epiphytes on productivity of Posidonia australis Hook. F.[J]. Aquatic Botany, 1986, 24(4): 355−371. doi: 10.1016/0304-3770(86)90102-6 [33] Irlandi E A, Orlando B A, Biber P D. Drift algae-epiphyte-seagrass interactions in a subtropical Thalassia testudinum meadow[J]. Marine Ecology Progress Series, 2004, 279: 81−91. doi: 10.3354/meps279081 [34] 张景平, 黄小平. 海草与其附生藻类之间的相互作用[J]. 生态学杂志, 2008, 27(10): 1785−1790.Zhang Jingping, Huang Xiaoping. Interactions between seagrass and its epiphytic algae: a review[J]. Chinese Journal of Ecology, 2008, 27(10): 1785−1790. [35] Jørgensen B B. Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments[J]. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 1982, 298(1093): 543−561. [36] Borum J, Pedersen O, Greve T M, et al. The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum[J]. Journal of Ecology, 2005, 93(1): 148−158. [37] Carlson Jr P R, Yarbro L A, Barber T R. Relationship of sediment sulfide to mortality of Thalassia testudinum in Florida Bay[J]. Bulletin of Marine Science, 1994, 54(3): 733−746. [38] Fischer-Piette E, Heim R, Lami R. Note préliminaire sur une maladie bactérienne des Zostères[J]. Comples rendues des séances de l'Académie des Sciences, 1932, 195: 1420−1422. [39] Den Hartog C. “Wasting disease” and other dynamic phenomena in Zostera beds[J]. Aquatic Botany, 1987, 27(1): 3−14. doi: 10.1016/0304-3770(87)90082-9 [40] Giesen W B J T, Van Katwijk M M, Den Hartog C. Temperature, salinity, insolation and wasting disease of eelgrass (Zostera marina L.) in the Dutch Wadden Sea in the 1930’s[J]. Netherlands Journal of Sea Research, 1990, 25(3): 395−404. doi: 10.1016/0077-7579(90)90047-K [41] Robblee M B, Barber T R, Carlson Jr P R, et al. Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay (USA)[J]. Marine Ecology Progress Series, 1991, 71: 297−299. doi: 10.3354/meps071297 [42] Hall M O, Furman B T, Merello M, et al. Recurrence of Thalassia testudinum seagrass die-off in Florida Bay, USA: initial observations[J]. Marine Ecology Progress Series, 2016, 560: 243−249. doi: 10.3354/meps11923 [43] Short F T, Ibelings B W, Den Hartog C. Comparison of a current eelgrass disease to the wasting disease in the 1930s[J]. Aquatic Botany, 1988, 30(4): 295−304. doi: 10.1016/0304-3770(88)90062-9 [44] Groner M L, Burge C A, Kim C J S, et al. Plant characteristics associated with widespread variation in eelgrass wasting disease[J]. Diseases of Aquatic Organisms, 2016, 118(2): 159−168. doi: 10.3354/dao02962 [45] Karling J S. The Plasmodiophorales[M]. 2nd ed. New York: Hafner Publishing Company, 1968: 37−92. [46] Veld W A M I, Rosendahl K C H M, Brouwer H, et al. Phytophthora gemini sp. nov., a new species isolated from the halophilic plant Zostera marina in the Netherlands[J]. Fungal Biology, 2011, 115(8): 724−732. doi: 10.1016/j.funbio.2011.05.006 [47] Govers L L, Veld W A M I, Meffert J P, et al. Marine Phytophthora species can hamper conservation and restoration of vegetated coastal ecosystems[J]. Proceedings of the Royal Society B, 2016, 283(1837): 20160812. doi: 10.1098/rspb.2016.0812 [48] Govers L L, Van Der Zee E M, Meffert J P, et al. Copper treatment during storage reduces Phytophthora and Halophytophthora infection of Zostera marina seeds used for restoration[J]. Scientific Reports, 2017, 7: 43172. doi: 10.1038/srep43172 [49] Kurilenko V V, Christen R, Zhukova N V, et al. Granulosicoccus coccoides sp. nov., isolated from leaves of seagrass (Zostera marina)[J]. International Journal of Systematic and Evolutionary Microbiology, 2010, 60(4): 972−976. doi: 10.1099/ijs.0.013516-0 [50] Sun Feifei, Zhang Xiaoli, Zhang Qianqian, et al. Seagrass (Zostera marina) colonization promotes the accumulation of diazotrophic bacteria and alters the relative abundances of specific bacterial lineages involved in benthic carbon and sulfur cycling[J]. Applied and Environmental Microbiology, 2015, 81(19): 6901−6914. doi: 10.1128/AEM.01382-15 [51] Garcias-Bonet N, Sherman T D, Duarte C M, et al. Distribution and pathogenicity of the protist Labyrinthula sp. in western Mediterranean seagrass meadows[J]. Estuaries and Coasts, 2011, 34(6): 1161−1168. doi: 10.1007/s12237-011-9416-4 [52] 黄道建, 黄小平. 海草污染生态学研究进展[J]. 海洋湖沼通报, 2007, 7(S1): 182−188.Huang Daojian, Huang Xiaoping. Researches on seagrass pollution ecology and their prospects[J]. Transactions of Oceanology and Limnolog, 2007, 7(S1): 182−188. [53] Dahl M, Deyanova D, Lyimo L D, et al. Effects of shading and simulated grazing on carbon sequestration in a tropical seagrass meadow[J]. Journal of Ecology, 2016, 104(3): 654−664. doi: 10.1111/1365-2745.12564 [54] Larkum A W D, Kendrick G A, Ralph P J. Seagrasses of Australia: Structure, Ecology and Conservation[M]. Cham: Springer, 2018: 1−797. [55] Thomson J A, Burkholder D A, Heithaus M R, et al. Extreme temperatures, foundation species, and abrupt ecosystem change: an example from an iconic seagrass ecosystem[J]. Global Change Biology, 2015, 21(4): 1463−1474. doi: 10.1111/gcb.12694 [56] Nielsen J T, Liesack W, Finster K. Desulfovibrio zosterae sp. nov., a new sulfate reducer isolated from surface-sterilized roots of the seagrass Zostera marina[J]. International Journal of Systematic Bacteriology, 1999, 49(2): 859−865. [57] Hassenrück C, Hofmann L C, Bischof K, et al. Seagrass biofilm communities at a naturally CO2-rich vent[J]. Environmental Microbiology Reports, 2015, 7(3): 516−525. doi: 10.1111/1758-2229.12282 [58] Devereux R. Seagrass rhizosphere microbial communities[M]//Kristensen E, Haese R R, Kostka J E. Coastal and Estuarine Studies: Interactions Between Macro and Microorganisms in Marine Sediments. American: American Geophysical Union, 2005: 199−216. [59] 凌娟, 董俊德, 张燕英, 等. 一株珊瑚礁−海草床复合生态系统固氮菌的分离与鉴定[J]. 微生物学通报, 2010, 37(7): 962−968.Ling Juan, Dong Junde, Zhang Yanying, et al. Isolation and characterization of a N2-fixing bacterium from coral reef-seagrass ecosystem[J]. Microbiology China, 2010, 37(7): 962−968. [60] 王琦, 李文涛, 张沛东, 等. 鳗草根际固氮菌的分离鉴定及培养条件的筛选[J]. 中国水产科学, 2017, 24(4): 791−801.Wang Qi, Li Wentao, Zhang Peidong, et al. Isolation and characterization of nitrogen-fixing bacteria in the rhiz-osphere of Zostera marina and optimization of its culture conditions[J]. Journal of Fishery Sciences of China, 2017, 24(4): 791−801. [61] Ling Juan, Zhang Yanying, Wu Meilin, et al. Fungal community successions in rhizosphere sediment of seagrasses Enhalus acoroides under PAHs stress[J]. International Journal of Molecular Sciences, 2015, 16(6): 14039−14055. [62] Stapel J, Aarts T L, Van Duynhoven B H M, et al. Nutrient uptake by leaves and roots of the seagrass Thalassia hemprichii in the Spermonde Archipelago, Indonesia[J]. Marine Ecology Progress Series, 1996, 134: 195−206. doi: 10.3354/meps134195 [63] Vohník M, Borovec O, Župan I, et al. Anatomically and morphologically unique dark septate endophytic association in the roots of the Mediterranean endemic seagrass Posidonia oceanica[J]. Mycorrhiza, 2015, 25(8): 663−672. doi: 10.1007/s00572-015-0642-7 [64] Venkatachalam A, Thirunavukkarasu N, Suryanarayanan T S. Distribution and diversity of endophytes in seagrasses[J]. Fungal Ecology, 2015, 13: 60−65. doi: 10.1016/j.funeco.2014.07.003 [65] Müller H, Berg C, Landa B B, et al. Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees[J]. Frontiers in Microbiology, 2015, 6: 138. [66] Cifuentes A, Antón J, Benlloch S, et al. Prokaryotic diversity in Zostera noltii-colonized marine sediments[J]. Applied and Environmental Microbiology, 2000, 66: 1715−1719. doi: 10.1128/AEM.66.4.1715-1719.2000 [67] Ling J, Lin X C, Zhang Y Y, et al. Community composition and transcriptional activity of ammonia-oxidizing prokaryotes of seagrass Thalassia hemprichii in coral reef ecosystems[J]. Frontiers in Microbiology, 2018, 9: 7. doi: 10.3389/fmicb.2018.00007 [68] Munn C B. Viruses as pathogens of marine organisms-from bacteria to whales[J]. Journal of the Marine Biological Association of the United Kingdom, 2006, 86(3): 453−467. doi: 10.1017/S002531540601335X [69] Luna G M, Corinaldesi C, Dell'Annob A, et al. Impact of aquaculture on benthic virus-prokaryote interactions in the Mediterranean Sea[J]. Water Research, 2013, 47(1): 1156−1168. [70] Van Bogaert N, Rosario K, Furman B T, et al. Discovery of a novel potexvirus in the seagrass Thalassia testudinum from Tampa Bay[J]. Limnology and Oceanography Letters, 2019, 4(1): 1−8. doi: 10.1002/lol2.10098 [71] Crump B C, Wojahn J M, Tomas F, et al. Metatranscriptomics and amplicon sequencing reveal mutualisms in seagrass microbiomes[J]. Frontiers in Microbiology, 2018, 9: 388. doi: 10.3389/fmicb.2018.00388 [72] Cúcio C, Engelen A H, Costa R, et al. Rhizosphere microbiomes of european + seagrasses are selected by the plant, but are not species specific[J]. Frontiers in Microbiology, 2016, 7: 440−448. [73] Hurtado-Mccormick V, Kahlke T, Petrou K, et al. Regional and microenvironmental scale characterization of the Zostera muelleri seagrass microbiome[J]. Frontiers in Microbiology, 2019, 10: 1011. doi: 10.3389/fmicb.2019.01011 [74] Kelly U, Laas P, Stingl U. The microbial communities of leaves and roots associated with turtle grass (Thalassia testudinum) and manatee grass (Syringodium filliforme) are distinct from seawater and sediment communities, but are similar between species and sampling sites[J]. Microorganisms, 2019, 7(1): 4. [75] Mejia A Y, Rotini A, Lacasella F, et al. Assessing the ecological status of seagrasses using morphology, biochemical descriptors and microbial community analyses. A study in Halophila stipulacea (Forsk.) Aschers meadows in the northern Red Sea[J]. Ecological Indicators, 2016, 60: 1150−1163. doi: 10.1016/j.ecolind.2015.09.014 [76] Ettinger C L, Voerman S E, Lang J M, et al. Microbial communities in sediment from Zostera marina patches, but not the Z. marina leaf or root microbiomes, vary in relation to distance from patch edge[J]. PeerJ, 2017, 5: e3246. doi: 10.7717/peerj.3246 [77] Uku J, Björk M, Bergman B, et al. Characterization and comparison of prokaryotic epiphytes associated with three east African seagrasses[J]. Phycology, 2007, 43(4): 768−779. doi: 10.1111/j.1529-8817.2007.00371.x [78] Panno L, Bruno M, Voyron S, et al. Diversity, ecological role and potential biotechnological applications of marine fungi associated to the seagrass Posidonia oceanica[J]. New Biotechnology, 2013, 30(6): 685−694. doi: 10.1016/j.nbt.2013.01.010 [79] Lindow S E, Brandl M T. Microbiology of the phyllosphere[J]. Applied and Environmental Microbiology, 2003, 69(4): 1875−1883. doi: 10.1128/AEM.69.4.1875-1883.2003 [80] Jankowska E, Jankowska K, Włodarska-Kowalczuk M. Seagrass vegetation and meiofauna enhance the bacterial abundance in the Baltic Sea sediments (Puck Bay)[J]. Environmental Science and Pollution Research, 2015, 22(18): 14372−14378. doi: 10.1007/s11356-015-5049-7 [81] Fahimipour A K, Kardish M R, Lang J M, et al. Global-scale structure of the eelgrass microbiome[J]. Applied and Environmental Microbiology, 2017, 83(12): e03391−16. [82] Bengtsson M M, Bühler A, Brauer A, et al. Eelgrass leaf surface microbiomes are locally variable and highly correlated with epibiotic eukaryotes[J]. Frontiers in Microbiology, 2017, 8: 1312. doi: 10.3389/fmicb.2017.01312 [83] Crump B C, Koch E W. Attached bacterial populations shared by four species of aquatic angiosperms[J]. Applied and Environmental Microbiology, 2008, 74(19): 5948−5957. doi: 10.1128/AEM.00952-08 [84] Corlett H, Jones B. Epiphyte communities on Thalassia testudinum from Grand Cayman, British West Indies: their composition, structure, and contribution to lagoonal sediments[J]. Sedimentary Geology, 2007, 194(3/4): 245−262. [85] Novak R. A study in ultra-ecology: microorganisms on the seagrass Posidonia oceanica (L.) DELILE[J]. Marine Ecology, 1984, 5(2): 143−190. doi: 10.1111/j.1439-0485.1984.tb00313.x [86] Celdrán D, Espinosa E, Sánchez-Amat A, et al. Effects of epibiotic bacteria on leaf growth and epiphytes of the seagrass Posidonia oceanica[J]. Marine Ecology Progress Series, 2012, 456: 21−27. doi: 10.3354/meps09672 [87] Kuo J. Morphology, anatomy and histochemistry of the Australian seagrasses of the genus Posidonia könig (Posidoniaceae). I. Leaf blade and leaf sheath of Posidonia australis Hook F.[J]. Aquatic Botany, 1978, 5: 171−190. doi: 10.1016/0304-3770(78)90060-8 [88] Steele L, Caldwell M, Boettcher A, et al. Seagrass-pathogen interactions: ‘pseudo-induction’ of turtlegrass phenolics near wasting disease lesions[J]. Marine Ecology Progress Series, 2005, 303: 123−131. doi: 10.3354/meps303123 [89] Brodersen K E, Nielsen D A, Ralph P J, et al. Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide[J]. New Phytologist, 2015, 205(3): 1264−1276. doi: 10.1111/nph.13124 [90] Frederiksen M S, Glud R N. Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study[J]. Limnology and Oceanography, 2006, 51(2): 1072−1083. doi: 10.4319/lo.2006.51.2.1072 [91] Blackburn T H, Nedwell D B, Wiebe W J. Active mineral cycling in a Jamaican seagrass sediment[J]. Marine Ecology Progress Series, 1994, 110(2/3): 233−239. [92] Jensen S I, Kühl M, Priemé A. Different bacterial communities associated with the roots and bulk sediment of the seagrass Zostera marina[J]. FEMS Microbiology Ecology, 2007, 62(1): 108−117. doi: 10.1111/j.1574-6941.2007.00373.x [93] Jiang Y F, Ling J, Wang Y S, et al. Cultivation-dependent analysis of the microbial diversity associated with the seagrass meadows in Xincun Bay, South China Sea[J]. Ecotoxicology, 2015, 24: 1540−1547. doi: 10.1007/s10646-015-1519-4 [94] Bourque A S, Kenworthy W J, Fourqurean J W. Impacts of physical disturbance on ecosystem structure in subtropical seagrass meadows[J]. Marine Ecology Progress Series, 2015, 540: 27−41. doi: 10.3354/meps11505 [95] Schulz B, Boyle C. What are Endophytes?[M]//Schulz B J E, Boyle C J C, Sieber T N. Microbial Root Endophytes. Soil Biology. Berlin, Heidelberg: Springer, 2006: 42−51. [96] Devarajan P T, Suryanarayanan T S, Geetha V. Endophytic fungi associated with the tropical seagrass Halophila ovalis (Hydrocharitaceae)[J]. Indian Journal of Geo-Marine Sciences, 2002, 31(1): 73−74. [97] Küsel K, Pinkart H C, Drake H L, et al. Acetogenic and sulfate-reducing bacteria inhabiting the rhizoplane and deep cortex cells of the sea grass halodule wrightii[J]. Applied and Environmental Microbiology, 1999, 65(11): 5117−5123. doi: 10.1128/AEM.65.11.5117-5123.1999 [98] Field C B, Behrenfeld M J, Randerson J T, et al. Primary production of the biosphere: integrating terrestrial and oceanic components[J]. Science, 1998, 281(5374): 237−240. doi: 10.1126/science.281.5374.237 [99] Blaabjerg V, Finster K. Sulphate reduction associated with roots and rhizomes of the marine macrophyte Zostera marina[J]. Aquatic Microbial Ecology, 1998, 15(3): 311−314. [100] Ugarelli K, Chakrabarti S, Laas P, et al. The seagrass holobiont and its microbiome[J]. Microorganisms, 2017, 5(4): 81. doi: 10.3390/microorganisms5040081 [101] Williams C J, Boyer J N, Jochem F J. Microbial activity and carbon, nitrogen, and phosphorus content in a subtropical seagrass estuary (Florida Bay): evidence for limited bacterial use of seagrass production[J]. Marine Biology, 2009, 156(3): 341−353. doi: 10.1007/s00227-008-1087-8 [102] Drake L A, Dobbs F C, Zimmerman R C. Effects of epiphyte load on optical properties and photosynthetic potential of the seagrasses Thalassia testudinum Banks ex König and Zostera marina L[J]. Limnology and Oceanography, 2003, 48(1): 456−463. [103] Holmer M, Andersen F Ø, Nielsen S L, et al. The importance of mineralization based on sulfate reduction for nutrient regeneration in tropical seagrass sediments[J]. Aquatic Botany, 2001, 71(1): 1−17. doi: 10.1016/S0304-3770(01)00170-X [104] 陈正浩, 张永雨, 杨素萍. 海洋玫瑰杆菌类群研究进展[J]. 生态学报, 2015, 35(5): 1620−1629.Chen Zhenghao, Zhang Yongyu, Yang Suping. Research progresses of marine Roseobacter lineage[J]. Acta Ecologica Sinica, 2015, 35(5): 1620−1629. [105] Welsh D T. Nitrogen fixation in seagrass meadows: regulation, plant-bacteria interactions and significance to primary productivity[J]. Ecology Letters, 2000, 3(1): 58−71. doi: 10.1046/j.1461-0248.2000.00111.x [106] Smith A C, Kostka J E, Devereux R, et al. Seasonal composition and activity of sulfate-reducing prokaryotic communities in seagrass bed sediments[J]. Aquatic Microbial Ecology, 2004, 37(2): 183−195. [107] McGlathery K J, Sundbäck K, Anderson I C. Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter[J]. Marine Ecology Progress Series, 2007, 348: 1−18. doi: 10.3354/meps07132 [108] Capone D G. Nitrogen fixation (acetylene reduction) by rhizosphere sediments of the eelgrass Zostera marina[J]. Marine Ecology Progress Series, 1982, 10(1): 67−75. [109] Vonk J A, Middelburg J J, Stapel J, et al. Dissolved organic nitrogen uptake by seagrasses[J]. Limnology and Oceanography, 2008, 53(2): 542−548. doi: 10.4319/lo.2008.53.2.0542 [110] Domingos P, Prado A M, Wong A, et al. Nitric oxide: a multitasked signaling gas in plants[J]. Molecular Plant, 2015, 8(4): 506−520. doi: 10.1016/j.molp.2014.12.010 [111] Caffrey J M, Kemp W M. Nitrogen cycling in sediments with estuarine populations of Potamogeton perfoliatus and Zostera marina[J]. Marine Ecology Progress Series, 1990, 66(1/2): 147−160. [112] Barrín C, Middelburg J J, Duarte C M. Phytoplankton trapped within seagrass (Posidonia oceanica) sediments are a nitrogen source: an in situ isotope labeling experiment[J]. Limnology and Oceanography, 2006, 51(4): 1648−1653. doi: 10.4319/lo.2006.51.4.1648 [113] Lehnen N, Marchant H K, Schwedt A, et al. High rates of microbial dinitrogen fixation and sulfate reduction associated with the Mediterranean seagrass Posidonia oceanica[J]. Systematic and Applied Microbiology, 2016, 39(7): 476−483. doi: 10.1016/j.syapm.2016.08.004 [114] Bagwell C E, La Rocque J R, Smith G W, et al. Molecular diversity of diazotrophs in oligotrophic tropical seagrass bed communities[J]. FEMS Microbiology Ecology, 2002, 39(2): 113−119. doi: 10.1111/j.1574-6941.2002.tb00912.x [115] Van Der Heide T, Govers L L, De Fouw J, et al. A three-stage symbiosis forms the foundation of seagrass ecosystems[J]. Science, 2012, 336(6087): 1432−1434. doi: 10.1126/science.1219973 [116] Moffler M D, Durako M J. Axenic culture of Thalassia testudinum banks ex könig (Hydrocharitaceae)[J]. American Journal of Botany, 1984, 71(10): 1455−1460. doi: 10.1002/j.1537-2197.1984.tb12004.x [117] Ross C, Puglisi M P, Paul V J. Antifungal defenses of seagrasses from the Indian River Lagoon, Florida[J]. Aquatic Botany, 2008, 88(2): 134−141. doi: 10.1016/j.aquabot.2007.09.003 [118] Marhaeni B, Radjasa O K, Bengen D G, et al. Screening of bacterial symbionts of seagrass Enhalus sp. against biofilm-forming bacteria[J]. Journal of Coastal Development, 2010, 13(2): 126−132. [119] Arnold T M, Tanner C E, Rothen M, et al. Wound-induced accumulations of condensed tannins in turtlegrass, Thalassia testudinum[J]. Aquatic Botany, 2008, 89(1): 27−33. doi: 10.1016/j.aquabot.2008.02.001 [120] Brearley A, Walker D I. Isopod miners in the leaves of two Western Australian Posidonia species[J]. Aquatic Botany, 1995, 52(3): 163−181. doi: 10.1016/0304-3770(95)00493-9 [121] Ofek-Lalzar M, Sela N, Goldman-Voronov M, et al. Niche and host-associated functional signatures of the root surface microbiome[J]. Nature Communications, 2014, 5: 4950. doi: 10.1038/ncomms5950 [122] Douglas A E, Werren J H. Holes in the hologenome: why host-microbe symbioses are not holobionts[J]. mBio, 2016, 7(2): e02099. [123] Hernandez-Agreda A, Leggat W, Bongaerts P, et al. The microbial signature provides insight into the mechanistic basis of coral success across reef habitats[J]. mBio, 2016, 7(4): e00560−16. [124] Toju H, Peay K G, Yamamichi M, et al. Core microbiomes for sustainable agroecosystems[J]. Nature Plants, 2018, 4(5): 247−257. doi: 10.1038/s41477-018-0139-4 [125] Astudillo-García C, Bell J J, Webster N S, et al. Evaluating the core microbiota in complex communities: a systematic investigation[J]. Environmental Microbiology, 2017, 19(4): 1450−1462. doi: 10.1111/1462-2920.13647 [126] Lemanceau P, Blouin M, Muller D, et al. Let the core microbiota be functional[J]. Trends in Plant Science, 2017, 22(7): 583−595. doi: 10.1016/j.tplants.2017.04.008 [127] Lundberg D S, Lebeis S L, Paredes S H, et al. Defining the core Arabidopsis thaliana root microbiome[J]. Nature, 2012, 4(7409): 86−90. [128] Kahlke T. Panbiom (Version 1.0)[Z]. San Francisco: GitHub Inc, 2017. [129] Coleman-Derr D, Desgarennes D, Fonseca G C, et al. Plant compartment and biogeography affect microbiome composition in cultivated and native agave species[J]. New Phytologist, 2016, 209(2): 798−811. doi: 10.1111/nph.13697 [130] Turner T R, James E K, Poole P S. The plant microbiome[J]. Genome Biology, 2013, 14(6): 209. doi: 10.1186/gb-2013-14-6-209 [131] Koch E W. Beyond light: physical, geological, and geochemical parameters as possible submersed aquatic vegetation habitat requirements[J]. Estuaries, 2001, 24(1): 1−17. doi: 10.2307/1352808 [132] Baden S, Gullström M, Lundén B, et al. Vanishing seagrass (Zostera marina, L.) in Swedish coastal waters[J]. AMBIO: A Journal of the Human Environment, 2003, 32(5): 374−377. doi: 10.1579/0044-7447-32.5.374 [133] Hasler-Sheetal H, Holmer M. Sulfide intrusion and detoxification in the seagrass Zostera marina[J]. PLoS One, 2015, 10(6): e0129136. doi: 10.1371/journal.pone.0129136 [134] Kirchman D L, Mazzella L, Alberte R S, et al. Epiphytic bacterial production on Zostera marina[J]. Marine Ecology Progress Series, 1984, 15(1/2): 117−123. [135] Dodd I C, Zinovkina N Y, Safronova V I, et al. Rhizobacterial mediation of plant hormone status[J]. Annals of Applied Biology, 2010, 157(3): 361−379. doi: 10.1111/j.1744-7348.2010.00439.x [136] Pinckney J L, Micheli F. Microalgae on seagrass mimics: does epiphyte community structure differ from live seagrasses[J]. Journal of Experimental Marine Biology and Ecology, 1998, 221(1): 59−70. doi: 10.1016/S0022-0981(97)00115-9 [137] 韩秋影, 张泽玉, 刘红霞, 等. 温度胁迫对日本鳗草(Zostera japonica)叶际可培养细菌的影响[J]. 生态学杂志, 2017, 36(9): 2564−2571.Han Qiuying, Zhang Zeyu, Liu Hongxia, et al. Effects of rising temperature on phyllosphere culturable bacteria of Zostera japonica[J]. Chinese Journal of Ecology, 2017, 36(9): 2564−2571. [138] Tout J, Siboni N, Messer L F, et al. Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis[J]. Frontiers in Microbiology, 2015, 6: 432.