Solène L Y Moulin, Sarah Frail, Thomas Braukmann, Jon Doenier, Melissa Steele-Ogus, Jane C Marks, Matthew M Mills, Ellen Yeh
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To identify the metabolic changes associated with this endosymbiotic specialization, we compared the <i>Epithemia</i> diazoplast with its close, free-living cyanobacterial relative, <i>Crocosphaera subtropica</i>. Unlike <i>C. subtropica</i>, in which nitrogenase activity is temporally separated from photosynthesis, we show that nitrogenase activity in the diazoplast is continuous through the day (concurrent with host photosynthesis) and night. Host and diazoplast metabolism are tightly coupled to support nitrogenase activity: Inhibition of photosynthesis abolishes daytime nitrogenase activity, while nighttime nitrogenase activity no longer requires cyanobacterial glycogen storage pathways. Instead, import of host-derived carbohydrates supports nitrogenase activity throughout the day-night cycle. Carbohydrate metabolism is streamlined in the diazoplast compared to <i>C. subtropica</i> with retention of the oxidative pentose phosphate pathway and oxidative phosphorylation. Similar to heterocysts, these pathways may be optimized to support nitrogenase activity, providing reducing equivalents and ATP and consuming oxygen. Our results demonstrate that the diazoplast is specialized for endosymbiotic nitrogen fixation. 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引用次数: 0
摘要
Epithemia spp.硅藻含有来自蓝藻的强制性固氮内共生体或重氮体。这些藻类是光合真核生物中成功将含氧光合作用与氧敏感的氮酶活性结合起来的罕见例子。在这里,我们报告了一个新分离出来的物种--克莱门特藻(E. clementina),并将其作为研究内共生获得固氮作用的模型。我们证明,失去光合作用的重氮质体向硅藻宿主提供固定氮以交换固定碳。为了确定与这种内共生特化相关的代谢变化,我们将重氮原生质表皮藻与其近亲、自由生活的蓝藻--亚热带栉水母(Crocosphaera subtropica)进行了比较。与亚热带蓝藻不同的是,重氮质体中的氮酶活动与光合作用在时间上是分离的,而我们的研究表明,重氮质体中的氮酶活动在白天(与寄主光合作用同时进行)和夜间都是持续进行的。宿主和重氮酵母的新陈代谢紧密耦合,以支持氮酶的活性:抑制光合作用会取消白天的氮酶活性,而夜间的氮酶活性不再需要蓝藻糖原储存途径。相反,在整个昼夜周期中,宿主碳水化合物的输入支持着氮酶的活性。与亚热带蓝藻相比,重氮藻体中的碳水化合物代谢得到了简化,保留了磷酸戊糖氧化途径和氧化磷酸化作用。与杂囊类似,这些途径可能经过优化,以支持氮酶活性,提供还原当量和 ATP 并消耗氧气。我们的研究结果表明,重氮质体专门用于内共生固氮。总之,我们建立了一个研究内共生的新模型,对这种重氮内共生进行了功能表征,并确定了内共生获得关键生物功能的代谢适应性。
The endosymbiont of Epithemia clementina is specialized for nitrogen fixation within a photosynthetic eukaryote.
Epithemia spp. diatoms contain obligate, nitrogen-fixing endosymbionts, or diazoplasts, derived from cyanobacteria. These algae are a rare example of photosynthetic eukaryotes that have successfully coupled oxygenic photosynthesis with oxygen-sensitive nitrogenase activity. Here, we report a newly-isolated species, E. clementina, as a model to investigate endosymbiotic acquisition of nitrogen fixation. We demonstrate that the diazoplast, which has lost photosynthesis, provides fixed nitrogen to the diatom host in exchange for fixed carbon. To identify the metabolic changes associated with this endosymbiotic specialization, we compared the Epithemia diazoplast with its close, free-living cyanobacterial relative, Crocosphaera subtropica. Unlike C. subtropica, in which nitrogenase activity is temporally separated from photosynthesis, we show that nitrogenase activity in the diazoplast is continuous through the day (concurrent with host photosynthesis) and night. Host and diazoplast metabolism are tightly coupled to support nitrogenase activity: Inhibition of photosynthesis abolishes daytime nitrogenase activity, while nighttime nitrogenase activity no longer requires cyanobacterial glycogen storage pathways. Instead, import of host-derived carbohydrates supports nitrogenase activity throughout the day-night cycle. Carbohydrate metabolism is streamlined in the diazoplast compared to C. subtropica with retention of the oxidative pentose phosphate pathway and oxidative phosphorylation. Similar to heterocysts, these pathways may be optimized to support nitrogenase activity, providing reducing equivalents and ATP and consuming oxygen. Our results demonstrate that the diazoplast is specialized for endosymbiotic nitrogen fixation. Altogether, we establish a new model for studying endosymbiosis, perform a functional characterization of this diazotroph endosymbiosis, and identify metabolic adaptations for endosymbiotic acquisition of a critical biological function.