A Type VI Secretion System Facilitates Fitness, Homeostasis, and Competitive Advantages for Environmental Adaptability and Efficient Nicotine Biodegradation
A Type VI Secretion System Facilitates Fitness, Homeostasis, and Competitive Advantages for Environmental Adaptability and Efficient Nicotine Biodegradation
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VI 型分泌系统促进健康、体内平衡和环境适应性和高效尼古丁生物降解的竞争优势
DOI：
10.1128/aem.03113-20
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发表时间：
2021-02
影响因子：
4.4
通讯作者：
Zhong Weihong
中科院分区：
文献类型：
--
作者：
Li Jun;Xie Linlin;Qian Shulan;Tang Yuhang;Shen Mingjie;Li Shanshan;Wang Jie;Xiong Lie;Lu Jie;Zhong Weihong
在不利的环境中，通常会发现各种污染物的混合物和多种生物的共存。关于含氮杂环污染物的生物降解，科学界通常集中于筛选将污染物转化为毒性减弱的中间体或用于初级代谢的功能酶。在这里，我们确定了T6 SS效应子TseN在假单胞菌菌株JY-Q中的双重作用，该菌株能够降解尼古丁。革兰氏阴性菌利用分泌系统将蛋白质效应物从细胞质转移到细胞外环境，从而与周围环境或微生物相互作用。已知细菌可以通过运输离子以对抗活性氧（ROS）而受益于VI型分泌系统（T6 SS）。在这里，我们报告说，T6 SS活动赋予耐受尼古丁诱导的氧化应激假单胞菌菌株JY-Q，一个高度活跃的尼古丁降解菌株从烟草废物提取物中分离出来。AA098_13375被鉴定为编码具有抗微生物和抗ROS活性的双功能效应子。野生型菌株JY-Q通过拮抗增加的细胞内ROS水平在含尼古丁的培养基中比AA098_13375缺失突变体生长得更好。因此，它被暂时命名为TseN（尼古丁耐受性的VI型分泌系统效应子），观察到其同系物在假单胞菌属物种中广泛存在。通过对细胞内NAD+的检测，TseN被鉴定为Tse 6样抑菌毒素。TseN对ROS表现出潜在的拮抗作用，以微调菌株JY-Q中尼古丁代谢的大量运输。由TseN驱动的NAD+的动态调节可以满足尼古丁降解的需求，同时具有较小的细胞毒性。在这种情况下，T6 SS涉及一个迷人的调节级联，通过提高细菌的鲁棒性/生长来促进N-杂环芳烃的组成性生物转化。总之，JY-Q中的T6 SS介导了对氧化应激的抗性，并通过接触非依赖性生长竞争优势促进了细菌适应性，此外还充分研究了T6 SS依赖性抗微生物活性。在不利的环境中，通常会发现各种污染物的混合物和多种生物的共存。关于含氮杂环污染物的生物降解，科学界通常集中于筛选将污染物转化为毒性减弱的中间体或用于初级代谢的功能酶。在这里，我们确定了T6 SS效应子TseN在假单胞菌菌株JY-Q中的双重作用，该菌株能够降解尼古丁。菌株JY-Q中的T6 SS能够递送TseN以杀死竞争者并通过非接触模式提供生长优势。TseN可以通过其水解酶活性监测细胞内NAD+水平，在竞争对手中引起细胞毒性，但在JY-Q上保持代谢稳态。免疫蛋白TsiN对JY-Q的毒性有保护作用。总之，我们发现TseN对细菌竞争者具有细胞毒性，促进JY-Q的尼古丁耐受性。因此，我们揭示了T6 SS和尼古丁代谢之间的工作模型。这一发现表明，细菌已经进化出多种多样的武器，以适应它们的生长和健壮性。
Mixtures of various pollutants and the coexistence of numerous species of organisms are usually found in adverse environments. Concerning biodegradation of nitrogen-heterocyclic contaminants, the scientific community has commonly focused on screening functional enzymes that transform pollutants into intermediates of attenuated toxicity or for primary metabolism. Here, we identified dual roles of the T6SS effector TseN in Pseudomonas sp. strain JY-Q, which is capable of degrading nicotine. ABSTRACT Gram-negative bacteria employ secretion systems to translocate proteinaceous effectors from the cytoplasm to the extracellular milieu, thus interacting with the surrounding environment or microniche. It is known that bacteria can benefit from the type VI secretion system (T6SS) by transporting ions to combat reactive oxygen species (ROS). Here, we report that T6SS activities conferred tolerance to nicotine-induced oxidative stress in Pseudomonas sp. strain JY-Q, a highly active nicotine degradation strain isolated from tobacco waste extract. AA098_13375 was identified to encode a dual-functional effector with antimicrobial and anti-ROS activities. Wild-type strain JY-Q grew better than the AA098_13375 deletion mutant in nicotine-containing medium by antagonizing increased intracellular ROS levels. It was, therefore, tentatively designated TseN (type VI secretion system effector for nicotine tolerance), homologs of which were observed to be broadly ubiquitous in Pseudomonas species. TseN was identified as a Tse6-like bacteriostatic toxin via monitoring intracellular NAD+. TseN presented potential antagonism against ROS to fine tune the heavy traffic of nicotine metabolism in strain JY-Q. It is feasible that the dynamic tuning of NAD+ driven by TseN could satisfy demands from nicotine degradation with less cytotoxicity. In this scenario, T6SS involves a fascinating accommodation cascade that prompts constitutive biotransformation of N-heterocyclic aromatics by improving bacterial robustness/growth. In summary, the T6SS in JY-Q mediated resistance to oxidative stress and promoted bacterial fitness via a contact-independent growth competitive advantage, in addition to the well-studied T6SS-dependent antimicrobial activities. IMPORTANCE Mixtures of various pollutants and the coexistence of numerous species of organisms are usually found in adverse environments. Concerning biodegradation of nitrogen-heterocyclic contaminants, the scientific community has commonly focused on screening functional enzymes that transform pollutants into intermediates of attenuated toxicity or for primary metabolism. Here, we identified dual roles of the T6SS effector TseN in Pseudomonas sp. strain JY-Q, which is capable of degrading nicotine. The T6SS in strain JY-Q is able to deliver TseN to kill competitors and provide a growth advantage by a contact-independent pattern. TseN could monitor the intracellular NAD+ level by its hydrolase activity, causing cytotoxicity in competitive rivals but metabolic homeostasis on JY-Q. Moreover, JY-Q could be protected from TseN toxicity by the immunity protein TsiN. In conclusion, we found that TseN with cytotoxicity to bacterial competitors facilitated the nicotine tolerance of JY-Q. We therefore reveal a working model between T6SS and nicotine metabolism. This finding indicates that multiple diversified weapons have been evolved by bacteria for their growth and robustness.
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影响因子：
64.8
作者：
通讯作者：
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影响因子：
7.7
作者：
Chih-Feng Wu;Yun-Wei Lien;Devanand Bondage;Jer-Sheng Lin;M. Pilhofer;Y. Shih;Jeff H. Chang;E. Lai-E.-La
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Chih-Feng Wu;Yun-Wei Lien;Devanand Bondage;Jer-Sheng Lin;M. Pilhofer;Y. Shih;Jeff H. Chang;E. Lai-E.-La
开发基于接合的高效假交替单胞菌遗传操作系统
影响因子：
6.4
作者：
Wang P;Yu Z;Li B;Cai X;Zeng Z;Chen X;Wang X
通讯作者：
Wang X
影响因子：
6.7
作者：
Cianfanelli FR;Alcoforado Diniz J;Guo M;De Cesare V;Trost M;Coulthurst SJ
通讯作者：
Coulthurst SJ
VI 型分泌系统通过分泌过氧化氢酶对抗宿主活性氧 (ROS)，从而增强肠出血性大肠杆菌的毒力
影响因子：
6.7
作者：
Wan B;Zhang Q;Ni J;Li S;Wen D;Li J;Xiao H;He P;Ou HY;Tao J;Teng Q;Lu J;Wu W;Yao YF
通讯作者：
Yao YF