How Thermophilic Gram-Positive Organisms Perform Extracellular Electron Transfer: Characterization of the Cell Surface Terminal Reductase OcwA
How Thermophilic Gram-Positive Organisms Perform Extracellular Electron Transfer: Characterization of the Cell Surface Terminal Reductase OcwA
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DOI：
10.1128/mbio.01210-19
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发表时间：
2019-07-01
期刊：
影响因子：
6.4
通讯作者：
Louro, R. O.
中科院分区：
文献类型：
--
作者：
Costa, N. L.;Hermann, B.;Louro, R. O.
细胞外电子传递是生物电化学系统发展的关键过程，是生产能量或附加值化合物的基础。ThermincolapotensJR是一种很有前途的革兰氏阳性细菌，用于这些系统，因为它是嗜热的。在本文中，我们描述的结构和功能特性的nonaheme细胞色素OcwA，这是终端还原酶的这种有机体。在2.2-A分辨率下确定的OcwA的结构表明，血红素的整体折叠和组织与其他金属还原酶无关，而是类似于参与氮和硫的生物化学循环的多血红素细胞色素。我们发现，除了固体电子受体，OcwA也可以减少可溶性电子穿梭和含氧阴离子。这些数据表明，OcwA可以作为一种多用途的呼吸酶，允许这种生物体在环境中生长，快速变化的终端电子受体的可用性，而不需要转录调控和蛋白质synthesization.IMPORTANCE嗜热革兰氏阳性生物体最近被证明是一个有前途的一类生物体被用于生产电能的生物电化学系统。这些生物体呈现厚的肽聚糖层，这被认为阻止它们进行细胞外电子转移（即，与细胞外的固体电子受体交换分解代谢电子）。在本文中，我们描述的结构和功能机制的多血红素细胞色素OcwA，在这种生物体的细胞表面发现的革兰氏阳性菌ThermincolapotensJR的末端还原酶。这里展示的结果表明，这种蛋白质可以发挥呼吸“瑞士军刀”的作用，使这种生物体在可溶性和不溶性底物的环境中生长。此外，它表明，它是无关的终端还原酶发现在细胞表面的其他电活性生物。相反，OcwA类似于可溶性电子受体的末端还原酶。我们的数据显示，可溶性和不溶性底物的末端氧化还原酶在进化上是相关的，为多血红素细胞色素的进化途径提供了新的见解。
Extracellular electron transfer is the key process underpinning the development of bioelectrochemical systems for the production of energy or addedvalue compounds. Thermincola potens JR is a promising Gram-positive bacterium to be used in these systems because it is thermophilic. In this paper, we describe the structural and functional properties of the nonaheme cytochrome OcwA, which is the terminal reductase of this organism. The structure of OcwA, determined at 2.2-A resolution, shows that the overall fold and organization of the hemes are not related to other metal reductases and instead are similar to those of multiheme cytochromes involved in the biogeochemical cycles of nitrogen and sulfur. We show that, in addition to solid electron acceptors, OcwA can also reduce soluble electron shuttles and oxyanions. These data reveal that OcwA can work as a multipurpose respiratory enzyme allowing this organism to grow in environments with rapidly changing availability of terminal electron acceptors without the need for transcriptional regulation and protein synthesis.IMPORTANCE Thermophilic Gram-positive organisms were recently shown to be a promising class of organisms to be used in bioelectrochemical systems for the production of electrical energy. These organisms present a thick peptidoglycan layer that was thought to preclude them to perform extracellular electron transfer (i.e., exchange catabolic electrons with solid electron acceptors outside the cell). In this paper, we describe the structure and functional mechanisms of the multiheme cytochrome OcwA, the terminal reductase of the Gram-positive bacterium Thermincola potens JR found at the cell surface of this organism. The results presented here show that this protein can take the role of a respiratory "Swiss Army knife," allowing this organism to grow in environments with soluble and insoluble substrates. Moreover, it is shown that it is unrelated to terminal reductases found at the cell surface of other electroactive organisms. Instead, OcwA is similar to terminal reductases of soluble electron acceptors. Our data reveal that terminal oxidoreductases of soluble and insoluble substrates are evolutionarily related, providing novel insights into the evolutionary pathway of multiheme cytochromes.