Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen.
Highly dynamic cellular-level response of symbiotic coral to a sudden increase in environmental nitrogen.
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DOI：
10.1128/mbio.00052-13
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发表时间：
2013-05-14
期刊：
影响因子：
6.4
通讯作者：
Meibom A
中科院分区：
文献类型：
--
作者：
Kopp C;Pernice M;Domart-Coulon I;Djediat C;Spangenberg JE;Alexander DT;Hignette M;Meziane T;Meibom A
与内共生光合甲藻共生藻的代谢相互作用。是造礁珊瑚（石珊瑚）在营养贫乏的热带海洋中繁衍生息的基础。然而，在单细胞水平上缺乏对这种基本共生关系中营养物质同化、易位和利用的详细了解。使用脉冲追踪 15N 标记和定量离子微探针同位素成像（NanoSIMS；纳米级二次离子质谱），我们在亚细胞水平上可视化了共生珊瑚 Pocillopora damicornis 组织中的这些动态过程。铵、硝酸盐和天冬氨酸的同化导致氮快速掺入尿酸晶体中（约 45 分钟后），在甲藻内共生体中形成临时氮存储位点。随后，该代谢物在细胞内重新动员，并伴随着含氮化合物易位至珊瑚宿主，从约 6 小时开始。在珊瑚组织内，氮在所有四种上皮细胞的特定细胞区室中被利用，包括粘液室、高尔基体和钙母细胞中的囊泡。我们的研究展示了氮限制共生珊瑚如何利用氮可用性的突然变化；这为不断变化的珊瑚礁环境中微生物共生中养分储存和再利用的功能研究开辟了新的视角。所采用的方法将透射电子显微镜与用稳定同位素示踪剂标记的珊瑚组织的纳米级二次离子质谱（NanoSIMS）成像相结合，可以对完整共生中的代谢通量进行量化和亚微米定位。这项研究为研究共生系统对养分可用性的生理适应以及增加对全球氮和碳生物地球化学循环的了解开辟了道路。
Metabolic interactions with endosymbiotic photosynthetic dinoflagellate Symbiodinium spp. are fundamental to reef-building corals (Scleractinia) thriving in nutrient-poor tropical seas. Yet, detailed understanding at the single-cell level of nutrient assimilation, translocation, and utilization within this fundamental symbiosis is lacking. Using pulse-chase 15N labeling and quantitative ion microprobe isotopic imaging (NanoSIMS; nanoscale secondary-ion mass spectrometry), we visualized these dynamic processes in tissues of the symbiotic coral Pocillopora damicornis at the subcellular level. Assimilation of ammonium, nitrate, and aspartic acid resulted in rapid incorporation of nitrogen into uric acid crystals (after ~45 min), forming temporary N storage sites within the dinoflagellate endosymbionts. Subsequent intracellular remobilization of this metabolite was accompanied by translocation of nitrogenous compounds to the coral host, starting at ~6 h. Within the coral tissue, nitrogen is utilized in specific cellular compartments in all four epithelia, including mucus chambers, Golgi bodies, and vesicles in calicoblastic cells. Our study shows how nitrogen-limited symbiotic corals take advantage of sudden changes in nitrogen availability; this opens new perspectives for functional studies of nutrient storage and remobilization in microbial symbioses in changing reef environments. The methodology applied, combining transmission electron microscopy with nanoscale secondary-ion mass spectrometry (NanoSIMS) imaging of coral tissue labeled with stable isotope tracers, allows quantification and submicrometric localization of metabolic fluxes in an intact symbiosis. This study opens the way for investigations of physiological adaptations of symbiotic systems to nutrient availability and for increasing knowledge of global nitrogen and carbon biogeochemical cycling.