Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation.
Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation.
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DOI：
10.1371/journal.pgen.1006490
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发表时间：
2016-12
期刊：
影响因子：
4.5
通讯作者：
Allen AE
中科院分区：
文献类型：
--
作者：
Smith SR;Gillard JT;Kustka AB;McCrow JP;Badger JH;Zheng H;New AM;Dupont CL;Obata T;Fernie AR;Allen AE
环境波动影响自然界中硅藻的分布、生长和丰度，其中铁（Fe）的可得性起着核心作用。硅藻对低铁响应的研究要么利用连续（24小时）照明，要么在一天的单一时间取样，缺少任何时间动态。我们分析了三角藻（Phaeodactylum tricornutum）在低、中、高溶解铁循环下的稳态生长过程中的生理、代谢物组成和全局转录本，以更好地了解在铁限制下生长的生理适应的遗传控制的基本方面。我们极大地扩展了参与低铁反应的基因目录，强调了铁限制硅藻细胞内运输的重要性。P. tricornutum表现出生长缓慢的转录组特征，导致细胞分裂/二氧化硅沉积时间延长，这可能影响铁限制区域的生物地球化学碳固存。在低铁条件下，光收获和核糖体生物发生转录物普遍减少，而参与铁获取和再循环的基因转录物水平则增加。我们还注意到，在低铁条件下生长的三角角藻中，支链氨基酸的合成和分解代谢增加的表达发生了变化，而参与核心代谢的基因的表达相对不受影响，这表明基本的细胞功能受到了保护。除了P. tricornutum对低铁的响应之外，我们还观察到初级和中级代谢的转录控制在光：暗循环中的主要协调变化，这有助于对独特硅藻途径（如线粒体糖酵解和鸟氨酸-尿素循环）的重要性有新的认识。本研究为硅藻生理和代谢在光暗循环中对铁可用性的转录调节提供了新的见解，为硅藻保持代谢平衡以快速响应铁输入的能力提供了机制理解，并揭示了其生态成功的策略。海洋硅藻生活在不断波动的环境中，它们必须适应这种环境才能生存。在阳光照射的时间里，光合作用发生，使硅藻能够储存能量，用于夜间维持能量需求。了解浮游植物生长调控的细胞和分子机制是很重要的，因为它们在食物网的基础上扮演着环境角色，并在调节大气中的碳通量。在海洋生态系统中，铁（Fe）的可用性通常会限制浮游植物的生长，当添加铁时，硅藻通常会胜过其他浮游植物，这表明它们具有适应性，使它们既能在低铁环境中生存，又能对铁的添加做出快速反应。这些适应可能是独特的，这取决于与沿海或海洋地区的隔离。为了确定适应策略，我们利用基因表达分析、代谢物和生理测量相结合的方法，描述了一种模式硅藻——三角褐藻（Phaeodactylum tricornutum）对昼夜循环中限制铁条件的反应。代谢和生长的主要协调变化在昼夜周期中被记录下来，低铁表达基因在暗期达到峰值。硅藻对限制铁的反应是增加铁的获取，而通过减慢细胞周期进程、减少能量获取和微妙的代谢重塑来降低生长速度。
Environmental fluctuations affect distribution, growth and abundance of diatoms in nature, with iron (Fe) availability playing a central role. Studies on the response of diatoms to low Fe have either utilized continuous (24 hr) illumination or sampled a single time of day, missing any temporal dynamics. We profiled the physiology, metabolite composition, and global transcripts of the pennate diatom Phaeodactylum tricornutum during steady-state growth at low, intermediate, and high levels of dissolved Fe over light:dark cycles, to better understand fundamental aspects of genetic control of physiological acclimation to growth under Fe-limitation. We greatly expand the catalog of genes involved in the low Fe response, highlighting the importance of intracellular trafficking in Fe-limited diatoms. P. tricornutum exhibited transcriptomic hallmarks of slowed growth leading to prolonged periods of cell division/silica deposition, which could impact biogeochemical carbon sequestration in Fe-limited regions. Light harvesting and ribosome biogenesis transcripts were generally reduced under low Fe while transcript levels for genes putatively involved in the acquisition and recycling of Fe were increased. We also noted shifts in expression towards increased synthesis and catabolism of branched chain amino acids in P. tricornutum grown at low Fe whereas expression of genes involved in central core metabolism were relatively unaffected, indicating that essential cellular function is protected. Beyond the response of P. tricornutum to low Fe, we observed major coordinated shifts in transcript control of primary and intermediate metabolism over light:dark cycles which contribute to a new view of the significance of distinctive diatom pathways, such as mitochondrial glycolysis and the ornithine-urea cycle. This study provides new insight into transcriptional modulation of diatom physiology and metabolism across light:dark cycles in response to Fe availability, providing mechanistic understanding for the ability of diatoms to remain metabolically poised to respond quickly to Fe input and revealing strategies underlying their ecological success. Oceanic diatoms live in constantly fluctuating environments to which they must adapt in order to survive. During sunlit hours, photosynthesis occurs allowing diatoms to store energy used at night to sustain energy demands. Cellular and molecular mechanisms for regulation of phytoplankton growth are important to understand because of their environmental roles at the base of food webs and in regulating carbon flux out of the atmosphere. In ocean ecosystems, the availability of iron (Fe) commonly limits phytoplankton growth and diatoms typically outcompete other phytoplankton when Fe is added, indicating they have adaptations allowing them to both survive at low Fe and rapidly respond to Fe additions. These adaptations may be unique depending on isolation from coastal or oceanic locations. To identify adaptive strategies, we characterized the response of a model diatom, Phaeodactylum tricornutum, to limiting Fe conditions over day:night cycles using a combination of gene expression analyses, metabolite, and physiology measurements. Major coordinated shifts in metabolism and growth were documented over diel cycles, with peak expression of low Fe expressed genes in the dark phase. Diatoms respond to limiting Fe by increasing Fe acquisition, while decreasing growth rate through slowed cell cycle progression, reduced energy acquisition, and subtle metabolic remodeling.
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影响因子：
4.8
作者：
Chatfield, Mark;Mander, Adrian
通讯作者：
Mander, Adrian
影响因子：
2.9
作者：
Brown, Kathryn L.;Twing, Katrina I.;Robertson, Deborah L.
通讯作者：
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DOI：
10.1073/pnas.1309345110
发表时间：
2013-12-17
影响因子：
11.1
作者：
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通讯作者：
Wolf-Gladrow, Dieter
影响因子：
64.8
作者：
Behrenfeld, Michael J.;Worthington, Kirby;Shea, Donald M.
通讯作者：
Shea, Donald M.
影响因子：
2.9
作者：
BERGES, JA;HARRISON, PJ
通讯作者：
HARRISON, PJ