Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine Trichodesmium
Mechanistic Model for the Coexistence of Nitrogen Fixation and Photosynthesis in Marine Trichodesmium
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DOI：
10.1128/msystems.00210-19
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发表时间：
2019-07-01
期刊：
影响因子：
6.4
通讯作者：
Deutsch, Curtis
中科院分区：
文献类型：
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作者：
Inomura, Keisuke;Wilson, Samuel T.;Deutsch, Curtis
蓝藻毛藻是向海洋表层提供新氮 (N) 的重要贡献者，但其保护固氮酶免受氧 (O-2) 抑制的策略仍知之甚少。我们提出了一个动态生理模型来评估假设的条件，使毛藻能够执行其两个相互冲突的代谢过程：N-2 固定和光合作用。首先，该模型表明管理细胞 O-2 以允许 N-2 固定需要高呼吸 O-2 消耗率。能量消耗相当于每日固定碳的 80%，与观察到的毛藻相对于其他浮游植物的生长速率的降低相当。其次，通过形成连接细胞的毛状体，毛藻可以将 N-2 固定与光合作用分开。储存的碳转移到固氮细胞会促进呼吸性 O-2 消耗，从而保护固氮酶，而新固定的氮到固碳细胞的相互转移则支持细胞生长。第三，尽管Trichodesmium缺乏异囊物种中发现的结构屏障，但该模型预测细胞膜的扩散率较低，这一功能可以通过革兰氏阴性膜的存在、细胞外多糖物质（EPS）的产生以及介入N-2固定细胞和光合细胞之间的“缓冲细胞”来解释。我们的研究结果表明，所有三个因素——呼吸保护、毛状体形成和扩散屏障——代表了重要的策略，尽管它们具有能量成本，但仍促进了寡营养需氧海洋中毛藻的生长，并使其成为新的活性氮的主要来源。 重要性 毛藻是一种主要的固氮蓝藻，对海洋氮循环具有重大影响。它也是实验室研究中广泛使用的模式生物。由于固氮酶固氮酶对氧气极其敏感，这些表面浮游生物如何管理固氮和光合作用这两个相互冲突的过程一直是一个长期存在的问题。在这项研究中，我们开发了一个简单的毛藻代谢通量模型，捕获观察到的光合作用、固氮和边界层氧浓度的日常循环。该模型表明，形成用于空间隔离固氮和光合作用的细胞链是必要的，但还不够。它还需要防止氧气扩散的屏障和通过呼吸进行高速率的氧气清除。最后，该模型表明细胞内氧气的寿命极短，从而使细胞在光合作用失活后立即形成低氧环境。
The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O-2) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditions that would allow Trichodesmium to carry out its two conflicting metabolic processes of N-2 fixation and photosynthesis. First, the model indicates that managing cellular O-2 to permit N-2 fixation requires high rates of respiratory O-2 consumption. The energetic cost amounts to similar to 80% of daily C fixation, comparable to the observed diminution of the growth rate of Trichodesmium relative to other phytoplankton. Second, by forming a trichome of connected cells, Trichodesmium can segregate N-2 fixation from photosynthesis. The transfer of stored C to N-fixing cells fuels the respiratory O-2 consumption that protects nitrogenase, while the reciprocal transfer of newly fixed N to C-fixing cells supports cellular growth. Third, despite Trichodesmium lacking the structural barrier found in heterocystous species, the model predicts low diffusivity of cell membranes, a function that may be explained by the presence of Gramnegative membrane, production of extracellular polysaccharide substances (EPS), and "buffer cells" that intervene between N-2-fixing and photosynthetic cells. Our results suggest that all three factors-respiratory protection, trichome formation, and diffusion barriers-represent essential strategies that, despite their energetic costs, facilitate the growth of Trichodesmium in the oligotrophic aerobic ocean and permit it to be a major source of new reactive nitrogen.IMPORTANCE Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates that the life span of intracellular oxygen is extremely short, thus enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis.