应用生态学报 ›› 2022, Vol. 33 ›› Issue (9): 2572-2584.doi: 10.13287/j.1001-9332.202209.031
王涛, 程珂珂, 蔡中华, 周进*
收稿日期:
2021-07-12
接受日期:
2022-05-09
出版日期:
2022-09-15
发布日期:
2023-03-15
通讯作者:
* E-mail: zhou.jin@sz.tsinghua.edu.cn
作者简介:
王 涛, 男, 1997年生, 硕士研究生。主要从事珊瑚微生物研究。E-mail: wangtao20 @mails.tsinghua.edu.cn
基金资助:
WANG Tao, CHENG Ke-ke, CAI Zhong-hua, ZHOU Jin*
Received:
2021-07-12
Accepted:
2022-05-09
Online:
2022-09-15
Published:
2023-03-15
摘要: “细菌-虫黄藻-珊瑚”是生态系统中一对经典的三角关系,其中包含着复杂的物质流、信息流和能量流,三者的平衡与稳定是维护珊瑚礁生态系统健康的重要保障。过去20年里针对共生体交互关系进行了大量研究,并取得了一些重要成果,明确了“细菌-虫黄藻-宿主”三者之间的物质代谢、营养交换以及与环境的交互关系。然而,基于共生系统的复杂性,一些现象背后的机制仍然未被充分揭示,尤其是共生体之间的通讯交流。信号分子介导的相互作用是珊瑚共生体稳态维持和高效运转的内在驱动力。本文以珊瑚共生体系中化学信号为重点,尝试梳理最新的研究进展,包括细菌与细菌、细菌与珊瑚、细菌与虫黄藻以及虫黄藻与珊瑚之间的通讯方式,重点关注了群体感应信号(QS)、二甲基巯基丙酸盐(DMSP)、糖类信号、脂类信号以及非编码RNA。选择性例举了QS信号介导的微生物协作和竞争、DMSP调节下的细菌和宿主的相互作用,以及环境胁迫下珊瑚和虫黄藻对非编码RNA的响应过程,强调了它们在共生体中的作用模式和生态意义。并对今后的研究重点和可能方向进行了提炼,包括研究维度的扩充、新技术-新方法的应用以及生态模型的构建等,旨在提升对三角关系互作方式的认识,增进对珊瑚共生体的理解,探索基于通讯语言的操纵方式为珊瑚礁生态系统的恢复和保护提供新思路。
王涛, 程珂珂, 蔡中华, 周进. 珊瑚共生体中“细菌-虫黄藻-宿主”三角关系的通讯交流[J]. 应用生态学报, 2022, 33(9): 2572-2584.
WANG Tao, CHENG Ke-ke, CAI Zhong-hua, ZHOU Jin. Research advances in communication interactions among the symbionts of “bacteria-zooxanthellae-coral”[J]. Chinese Journal of Applied Ecology, 2022, 33(9): 2572-2584.
[1] Zoccola D, Ounais N, Barthelemy D, et al. The World Coral Conservatory (WCC): A Noah’s ark for corals to support survival of reef ecosystems. PLoS Biology, 2020, 18(9): e3000823 [2] Sorokin YI. Coral Reef Ecology. Berlin: Springer-Verlag, 1993: 1-3 [3] Oppen MJHV, Blackall LL. Coral microbiome dynamics, functions and design in a changing world. Nature Reviews Microbiology, 2019, 17: 557-567 [4] Peixoto RS, Rosado PM, Assis LDCD, et al. Beneficial microorganisms for corals (BMC): Proposed mechanisms for coral health and resilience. Frontiers in Microbiology, 2017, 8: 341 [5] 汤开浩, 王嫣, 王晓雪. 造礁珊瑚共附生微生物信号分子的研究进展. 中国科学: 地球科学, 2019, 49(5): 753-764 [6] 林姿君, 杜小鹏, 曾艳华, 等. 珊瑚共生细菌稳定性调节机制研究进展. 应用与环境生物学报, 2020, 26(4): 857-866 [7] Rosset SL, Oakley CA, Ferrior-Pagès C, et al. The molecular language of the cnidarian-dinoflagellate symbiosis. Trends in Microbiology, 2020, 29: 320-333 [8] Matthews JL, Crowder CM, Oakley CA, et al. Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114: 13194-13199 [9] Kaiser D, Losick R. How and why bacteria talk to each other. Cell, 1993, 73: 873-885 [10] Padder SA, Prasad R, Shah AH. Quorum sensing: A less known mode of communication among fungi. Microbiological Research, 2018, 210: 51-58 [11] Cude WN, Buchan A. Acyl-homoserine lactone-based quorum sensing in the Roseobacter clade: Complex cell-to-cell communication controls multiple physiologies. Frontiers in Microbiology, 2013, 4: 336, doi: 10.3389/fmicb.2013.00336 [12] 林姿君. 鹿角珊瑚中群体感应细菌的筛选及其对白化的介导作用. 硕士论文. 北京: 清华大学, 2019 [13] Tait K, Hutchison Z, Thompson FL, et al. Quorum sensing signal production and inhibition by coral-associated vibrios. Environmental Microbiology Reports, 2010, 2: 145-150 [14] Certner RH, Vollmer SV. Evidence for autoinduction and quorum sensing in white band disease causing microbes on Acropora cervicornis. Scientific Reports, 2015, 5(1): 11134, doi: 10.1038/srep11134 [15] Zhou J, Lin ZJ, Cai ZH, et al. Opportunistic bacteria use quorum sensing to disturb coral symbiotic communities and mediate the occurrence of coral bleaching. Environmental Microbiology, 2020, 22: 1944-1962 [16] Munn CB. The role of Vibrios in diseases of corals. Microbiology Spectrum, 2015, 3: VE-0006-2014 [17] Tello E, Castellanos L, Arévalo-Ferro C, et al. Disruption in quorum-sensing systems and bacterial biofilm inhibition by cembranoid diterpenes isolated from the octocoral Eunicea knighti. Journal of Natural Products, 2012, 75: 1637-1642 [18] Certner RH, Vollmer SV. Inhibiting bacterial quorum sensing arrests coral disease development and disease-associated microbes. Environmental Microbiology, 2018, 20: 645-657 [19] Alagely A, Krediet CJ, Ritchie KB, et al. Signaling mediated cross-talk modulates swarming and biofilm formation in a coral pathogen Serratia marcescens. The ISME Journal, 2011, 5: 1609-1620 [20] Teplitski M, Warriner K, Bartz J, et al. Untangling metabolic and communication networks: Interactions of Enterics with phytobacteria and their implications in produce safety. Trends in Microbiology, 2011, 19: 121-127 [21] Skindersoe ME, Ettinger-Epstein P, Rasmussen TB, et al. Quorum sensing antagonism from marine organisms. Marine Biotechnology, 2008, 10: 56-63 [22] Rajamani S, Bauer WD, Robinson JB, et al. The vitamin riboflavin and its derivative lumichrome activate the LasR bacterial quorum-sensing receptor. Molecular Plant-Microbe Interactions, 2008, 21: 1184-1192 [23] Cleo P, Christian T, Sylvain F, et al. Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114: E8488-E8497 [24] Van DWJAJM , Allemand D, Ferrier-Pagès C. Host-microbe interactions in octocoral holobionts-recent advances and perspectives. Microbiome, 2018, 6: 64 [25] Wheeler GL, Tait K, Taylor A, et al. Acylhomoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant, Cell and Environment, 2006, 29: 608-618 [26] Zimmer BL, May AL, Bhedi CD, et al. Quorum sensing signal production and microbial interactions in a polymicrobial disease of corals and the coral surface mucopolysaccharide layer. PLoS One,2014, 9(9): e108541 [27] Raina JB, Tapiolas D, Forêt S, et al. DMSP biosynthesis by an animal and its role in coral thermal stress response. Nature, 2013, 502: 677-680 [28] Tout J, Jeffries TC, Petrou K, et al. Chemotaxis by natural populations of coral reef bacteria. The ISME Journal, 2015, 9: 1764-1777 [29] Raina JB, Dinsdale EA, Willis BL, et al. Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends in Microbiology, 2010, 18: 101-108 [30] Garren M, Son K, Raina JB, et al. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. The ISME Journal, 2014, 8: 999-1007 [31] Patra SK, Samaddar S, Sinha N, et al. Reactive nitrogen species induced catalases promote a novel nitrosative stress tolerance mechanism in Vibrio cholerae. Nitric Oxide-Biology and Chemistry, 2019, 88: 35-44 [32] Wang CY, Wang KL, Qian PY, et al. Antifouling phenyl ethers and other compounds from the invertebrates and their symbiotic fungi collected from the South China Sea. AMB Express, 2016, 6: 1-10 [33] Pham TM, Wiese J, Wenzel-Storjohann A, et al. Diversity and antimicrobial potential of bacterial isolates associated with the soft coral Alcyonium digitatum from the Baltic Sea. Antonie Van Leeuwenhoek, 2016, 109: 105-119 [34] Elahwany AMD, Ghozlan HA, Elsharif HA, et al. Phylogenetic diversity and antimicrobial activity of marine bacteria associated with the soft coral Sarcophyton glaucum. Journal of Basic Microbiology, 2015, 55: 2-10 [35] Williams GC, Chen JY. Resurrection of the octocorallian genus Antillogorgia for Caribbean species previously assigned to Pseudopterogorgia, and a taxonomic assessment of the relationship of these genera with Leptogorgia (Cnidaria, Anthozoa, Gorgoniidae). Zootaxa, 2012, 3505: 39-52 [36] Karthik L, Li Z. Biosynthesis of antibiotics from microbial symbionts of sponges and corals// Loganathan K, ed. Symbiotic Microbiomes of Coral Reefs Sponges and Corals. Dordrecht: Springer, 2019: 249-261 [37] 杨静明, 杨文聪, 刘亚月, 等. 化学诱导对一株海洋来源土曲霉C23-3次生代谢产物及其生物活性的影响. 微生物学通报, 2019, 46(3): 441-452 [38] 郭秀春, 郑立, 崔志松, 等. 海绵共栖细菌NJ6-3-1基于群体感应调控的抗菌活性. 微生物学通报, 2008, 48(4): 545-550 [39] 周进, 晋慧, 蔡中华. 微生物在珊瑚礁生态系统中的作用与功能. 应用生态学报, 2014, 25(3): 919-930 [40] Seymour JR, Simó R, Ahmed T, et al. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science, 2010, 329: 342-345 [41] Guibert I, Bourdreux F, Bonnard I. et al. Dimethylsulfoniopropionate concentration in coral reef invertebrates varies according to species assemblages. Scientific Reports, 2020, 10: 9922 [42] Geng HF, Belas R. Molecular mechanisms underlying roseobacter-phytoplankton symbioses. Current Opinion in Biotechnology, 2010, 21: 332-338 [43] Davidson SK, Koropatnick TA, Kossmehl R, et al. NO means ‘yes’ in the squid-vibrio symbiosis: Nitric oxide (NO) during the initial stages of a beneficial association. Cellular Microbiology, 2004, 6: 1139-1151 [44] Plate L, Marletta MA. Nitric oxide-sensing H-NOX proteins govern bacterial communal behavior. Trends in Biochemical Sciences, 2013, 38: 566-575 [45] Barry M. Genetic recombination in Rhodopseudomonas capsulata. Proceedings of the National Academy of Sciences of the United States of America, 1974, 71: 971-973 [46] Luo HW, Moran MA. Evolutionary ecology of the marine Roseobacter clade. Microbiology and Molecular Biology Review, 2014, 78: 573-587 [47] Tooba V, Ana PBM, Arthur WSL, et al. Genomic repertoire of Mameliella alba Ep20 associated with Symbiodinium from the endemic coral Mussismilia braziliensis. Symbiosis, 2020, 80: 53-60 [48] Parkinson JE, Tivey TR, Mandelare PE, et al. Subtle differences in symbiont cell surface glycan profiles do not explain species-specific colonization rates in a model cnidarian-algal symbiosis. Frontiers in Microbiology, 2018, 9: 842-854 [49] Kitchen SA, Weis VM. The sphingosine rheostat is involved in the cnidarian heat stress response but not necessarily in bleaching. Journal of Experimental Biology, 2017, 220: 1709-1720 [50] Hambleton EA, Jones VAS, Maegele I, et al. Sterol transfer by atypical cholesterol-binding NPC2 proteins in coral-algal symbiosis. eLife, 2019, 8: e43923 [51] Marangoni LFB, Mies M, Guth AZ, et al. Peroxynitrite generation and increased heterotrophic capacity are linked to the disruption of the coral-dinoflagellate symbiosis in a scleractinian and hydrocoral species. Microorganisms, 2019, 7: 426 [52] Baumgarten S, Cziesielski MJ, Thomas L, et al. Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis. Molecular Ecology, 2018, 27: 403-418 [53] 杨潇湘, 张蕾, 黄小琴, 等. 基于高通量测序分析大豆和油菜根际微生物群落结构的差异. 应用生态学报, 2019, 30(7): 2345-2351 [54] Varki A. Biological roles of glycans. Glycobiology, 2017, 27: 3-49 [55] Kuniya N, Jimbo M, Tanimoto F, et al. Possible involvement of Tachylectin-2-like lectin from Acropora tenuis in the process of Symbiodinium acquisition. Fisheries Science, 2015, 81: 473-483 [56] Meints RH, Pardy RL. Quantitative demonstration of cell surface involvement in a plant-animal symbiosis: Lectin inhibition of reassociation. Journal of Cell Science, 1980, 43: 239-251 [57] Dennis EA, Norris PC. Eicosanoid storm in infection and inflammation. Nature Reviews Immunology, 2015, 15: 511-523 [58] Niu M, Keller NP. Co-opting oxylipin signals in microbial disease. Cellular Microbiology, 2019, 21: e13025 [59] Deboever E, Deleu M, Mongrand S, et al. Plant-pathogen interactions: Underestimated roles of phyto-oxylipins. Trends in Plant Science, 2020, 25: 22-34 [60] Lõhelaid H, Samel N. Eicosanoid diversity of stony corals. Marine Drugs, 2018, 16(1): 10 [61] Lawson CA, Possell M, Seymour JR, et al. Coral endosymbionts (Symbiodiniaceae) emit species-specific volatilomes that shift when exposed to thermal stress. Scientific Reports, 2019, 9: 17395 [62] Hannun YA, Obeid LM. Sphingolipids and their metabolism in physiology and disease. Nature Reviews Molecular Cell Biology, 2018, 19: 175-191 [63] Rolando M, Escoll P, Nora T, et al. Legionella pneumophila S1P-lyase targets host sphingolipid metabolism and restrains autophagy. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113: 1901-1906 [64] Ali U, Li HH, Wang XM, et al. Emerging roles of sphingolipid signaling in plant response to biotic and abiotic stresses. Molecular Plant, 2018, 11: 1328-1343 [65] Luttgeharm KD, Chen M, Mehra A, et al. Overexpression of arabidopsis ceramide synthases differentially affects growth, sphingolipid metabolism, programmed cell death, and mycotoxin resistance. Plant Physiology, 2015, 169: 1108-1117 [66] Rodriguez-Lanetty M, Phillips WS, Weis VM, et al. Transcriptome analysis of a cnidarian-dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics, 2006, 7: 23 [67] Detournay O, Weis VM. Role of the sphingosine rheostat in the regulation of cnidarian-dinoflagellate symbioses. The Biological Bulletin, 2011, 221: 261-269 [68] Wollam J, Antebi A. Sterol regulation of metabolism, homeostasis, and development. Annual Review of Biochemistry, 2011, 80: 885-916 [69] Baumgarten S, Simakov O, Esherick LY, et al. The genome of Aiptasia, a sea anemone model for coral symbiosis. Proceedings of the National Academy of Sciences of the United States of America, 2015,112: 11893-11898 [70] Dani V, Priouzeau F, Mertz M, et al. Expression patterns of sterol transporters NPC1 and NPC2 in the cnidarian-dinoflagellate symbiosis. Cellular Microbiology, 2017, 19: e12753 [71] Manes S, Real DG, Martinez AC, et al. Pathogens: Raft hijackers. Nature Reviews Immunology, 2003, 3: 557-568 [72] Paul S, Roychoudhury A. Regulation of physiological aspects in plants by hydrogen sulfide and nitric oxide under challenging environment. Physiologia Plantarum, 2020, 168: 374-393 [73] Cortese-Krott MM, Koning A, Kuhnle GGC, et al. The reactive species interactome: Evolutionary emergence, biological significance, and opportunities for redox metabolomics and personalized medicine. Antioxidants and Redox Signaling, 2017, 27: 684-712 [74] Suggett DJ, Smith DJ. Coral bleaching patterns are the outcome of complex biological and environmental networking. Global Chang Biology, 2020, 26: 68-79 [75] Peleg-Grossman S, Melamed-Book N, Levine A, et al. ROS production during symbiotic infection suppresses pathogenesis-related gene expression. Plant Signaling and Behavior, 2012, 7: 409-415 [76] Hawkins TD, Krueger T, Becker S, et al. Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals. Coral Reefs, 2014, 33: 141-153 [77] Weiberg A, Bellinger M, Jin HL, et al. Conversations between kingdoms: Small RNAs. Current Opinion Biotechnology, 2015, 32: 207-215 [78] Xu YJ, Zhu SW, Liu F, et al. Identification of arbuscular mycorrhiza fungi responsive microRNAs and their regulatory network in maize. International Journal of Molecular Sciences, 2018, 19: 1-13 [79] Lin SJ, Cheng SF, Song B, et al. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science, 2015, 350: 691-694 [80] Ware JR, Smith SV, Reaka-Kudla ML. Coral reefs: Sources or sinks of atmospheric CO2? Coral Reefs, 1992, 11: 127-130 [81] Macreadie PI, Anton A, Raven JA, et al. The future of blue carbon science. Nature Communications, 2019, 10: 1-13 [82] 石拓, 郑新庆, 张涵, 等. 珊瑚礁: 减缓气候变化的潜在蓝色碳汇. 中国科学院院刊, 2021, 36(3): 270-278 |
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