Deep-Sea Bacterium Shewanella piezotolerans WP3 Has Two Dimethyl Sulfoxide Reductases in Distinct Subcellular Locations
Deep-Sea Bacterium Shewanella piezotolerans WP3 Has Two Dimethyl Sulfoxide Reductases in Distinct Subcellular Locations
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深海细菌 Shewanella piezotolerans WP3 在不同的亚细胞位置有两个二甲亚砜还原酶
DOI：
10.1128/aem.01262-17
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发表时间：
2017-09-01
影响因子：
4.4
通讯作者：
Xiao，Xiang
中科院分区：
文献类型：
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作者：
Xiong，Lei;Jian，Huahua;Xiao，Xiang
摘要二甲基亚砜(DMSO)是深海中二甲基硫(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。从西太平洋深海沉积物中分离到Pop3希瓦氏菌，在4℃/20 Mpa的原位条件下，两个功能正常的DMSO呼吸系统对WP3的最大生长是必不可少的。然而，这两个子系统之间的关系和WP3还原DMSO的电子传递途径仍不清楚。在这项研究中，WP3中的两种DMSO还原酶(类型I和类型VI)被发现在功能上是独立的，尽管它们之间有着密切的进化关系。此外，DMSO还原酶亚基的免疫金标记法显示，I型DMSO还原酶位于外膜的外叶，而VI型DMSO还原酶位于周质间隙。CymA是一种细胞质结合的四氢血红素c型细胞色素，是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。在这些结果的基础上，我们提出了深海细菌DMSO还原的核心电子传递模型。这些结果表明，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DMSO利用的一种适应策略。二甲基亚砜(DMSO)作为深海中主要的甲基化硫化物，在挥发性抗温室气体二甲基硫(DMS)的海洋生物地球化学循环中发挥着重要作用。深海细菌希瓦氏杆菌WP3中的两组DMSO呼吸系统先前已被鉴定为在原位条件下(4℃/20兆帕)介导DMSO还原。在这里，我们报道了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厌氧呼吸系统在底栖微生物中的适应机制。
ABSTRACT 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.