Dimethyl sulfoxide (DMSO) acts as a substantial sink for dimethyl sulfide (DMS) in deep waters and is therefore considered a potential electron acceptor supporting abyssal ecosystems. Shewanella piezotolerans WP3 was isolated from west Pacific deep-sea sediments, and two functional DMSO respiratory subsystems are essential for maximum growth of WP3 under in situ conditions (4°C/20 MPa). However, the relationship between these two subsystems and the electron transport pathway underlying DMSO reduction by WP3 remain unknown. In this study, both DMSO reductases (type I and type VI) in WP3 were found to be functionally independent despite their close evolutionary relationship. Moreover, immunogold labeling of DMSO reductase subunits revealed that the type I DMSO reductase was localized on the outer leaflet of the outer membrane, whereas the type VI DMSO reductase was located within the periplasmic space. CymA, a cytoplasmic membrane-bound tetraheme c-type cytochrome, served as a preferential electron transport protein for the type I and type VI DMSO reductases, in which type VI accepted electrons from CymA in a DmsE- and DmsF-independent manner. Based on these results, we proposed a core electron transport model of DMSO reduction in the deep-sea bacterium S. piezotolerans WP3. These results collectively suggest that the possession of two sets of DMSO reductases with distinct subcellular localizations may be an adaptive strategy for WP3 to achieve maximum DMSO utilization in deep-sea environments.IMPORTANCE As the dominant methylated sulfur compound in deep oceanic water, dimethyl sulfoxide (DMSO) has been suggested to play an important role in the marine biogeochemical cycle of the volatile anti-greenhouse gas dimethyl sulfide (DMS). Two sets of DMSO respiratory systems in the deep-sea bacterium Shewanella piezotolerans WP3 have previously been identified to mediate DMSO reduction under in situ conditions (4°C/20 MPa). Here, we report that the two DMSO reductases (type I and type VI) in WP3 have distinct subcellular localizations, in which type I DMSO reductase is localized to the exterior surface of the outer membrane and type VI DMSO reductase resides in the periplasmic space. A core electron transport model of DMSO reduction in WP3 was constructed based on genetic and physiological data. These results will contribute to a comprehensive understanding of the adaptation mechanisms of anaerobic respiratory systems in benthic microorganisms.

中文翻译：

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深海细菌 Shewanella piezotolerans WP3 在不同的亚细胞位置具有两种二甲亚砜还原酶。


二甲亚砜 (DMSO) 在深水中充当二甲硫醚 (DMS) 的重要汇，因此被认为是支持深海生态系统的潜在电子受体。 Shewanella piezotolerans WP3 是从西太平洋深海沉积物中分离出来的，两个功能性 DMSO 呼吸子系统对于 WP3 在原位条件（4°C/20 MPa）下的最大生长至关重要。然而，这两个子系统与 WP3 还原 DMSO 的电子传递途径之间的关系仍然未知。在这项研究中，发现 WP3 中的两种 DMSO 还原酶（I 型和 VI 型）尽管进化关系密切，但在功能上是独立的。此外，DMSO还原酶亚基的免疫金标记显示，I型DMSO还原酶位于外膜的外叶上，而VI型DMSO还原酶位于周质空间内。 CymA 是一种细胞质膜结合的四血红素 c 型细胞色素，作为 I 型和 VI 型 DMSO 还原酶的优先电子传递蛋白，其中 VI 型以不依赖于 DmsE 和 DmsF 的方式接受来自 CymA 的电子。基于这些结果，我们提出了深海细菌 S. piezotolerans WP3 中 DMSO 还原的核心电子传输模型。这些结果共同表明，拥有两组具有不同亚细胞定位的 DMSO 还原酶可能是 WP3 在深海环境中实现最大程度利用 DMSO 的适应性策略。 重要性 作为深海水中主要的甲基化硫化合物，二甲亚砜（ DMSO）已被认为在挥发性抗温室气体二甲硫醚（DMS）的海洋生物地球化学循环中发挥着重要作用。 深海细菌 Shewanella piezotolerans WP3 中的两套 DMSO 呼吸系统先前已被确定可在原位条件（4°C/20 MPa）下介导 DMSO 还原。在这里，我们报道WP3中的两种DMSO还原酶（I型和VI型）具有不同的亚细胞定位，其中I型DMSO还原酶定位于外膜的外表面，VI型DMSO还原酶位于周质空间。基于遗传和生理数据，构建了 WP3 中 DMSO 还原的核心电子传递模型。这些结果将有助于全面了解底栖微生物厌氧呼吸系统的适应机制。