产酶溶杆菌：“一位全副武装的生防战士”

doi:10.1016/j.jia.2024.02.021

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (1): 23-35.DOI: 10.1016/j.jia.2024.02.021

产酶溶杆菌：“一位全副武装的生防战士”

收稿日期:2023-11-30 接受日期:2024-01-29 出版日期:2025-01-20 发布日期:2025-01-06

Lysobacter enzymogenes: A fully armed biocontrol warrior

Long Lin¹, Xiaolong Shao¹, Yicheng Yang¹, Aprodisia Kavutu Murero¹, Limin Wang¹, Gaoge Xu², Yangyang Zhao², Sen Han³, Zhenhe Su³, Kangwen Xu⁴, Mingming Yang⁵, Jinxing Liao⁶, Kaihuai Li⁷, Fengquan Liu^{2, 7#}, Guoliang Qian^1#

¹Key Laboratory of Integrated Management of Crop Diseases and Pests/College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China
²Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China
³Integrated Pest Management Innovation Center of Hebei Province, Plant Protection Institute, Hebei Academy of Agriculture and Forestry Sciences, Baoding 071000, China
⁴Marine Agriculture Research Center, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
⁵College of Plant Protection, Northwest A&F University, Yangling 712100, China
⁶Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Plant Pests, College of Plant Protection, Hunan Agricultural University, Changsha 410128, China
⁷Department of Plant Pathology, College of Agriculture, Guizhou University, Guiyang 550025, China

Received:2023-11-30 Accepted:2024-01-29 Online:2025-01-20 Published:2025-01-06
About author:#Correspondence Guoliang Qian, Tel: +86-25-84396109, E-mail: glqian@njau.edu.cn; Fengquan Liu, Tel: +86-25-84390277, E-mail: fqliu20011@sina.com
Supported by:
Research on L. enzymogenes was funded by the the Fundamental Research Funds for the Central Universities, China (RENCAI2024002 and KJJQ2024014), the Natural Key Research and Development Program of China (2022YFD1400200), and the National Natural Science Foundation of China (U22A20486, 32072470, 32001955 and 32470112).

摘要/Abstract

摘要：

产酶溶杆菌是一种新型的生防细菌，能产生胞外水解酶、抗真菌毒素蛋白、抗菌次生代谢产物、IV型分泌系统（T4SS）等多种生防武器，高效抑制真菌、卵菌、细菌、线虫等多种植物病原菌的生长。与常见的生防假单胞菌和芽胞杆菌相比，产酶溶杆菌具备一些独特的生防特征，例如细胞表面缺乏鞭毛，可合成并分泌新型抗真菌代谢产物HSAF（heat-stable antifungal factor，宁溶霉素），通过T4SS接触抑制病原细菌的生长等。本文将重点从丢失鞭毛的形态和功能适应性，抗真菌代谢产物HSAF的合成调控机制，T4SS介导“接触抑菌”三个方面阐述产酶溶杆菌具备这些独特生防特性背后的机制。研究表明，产酶溶杆菌基因组中部分鞭毛合成相关基因缺失导致其丢失鞭毛，但依然保留鞭毛III型分泌系统。该系统在产酶溶杆菌中不再负责鞭毛合成，而是发生功能分化，参与IV型菌毛合成以及抗真菌毒素蛋白的分泌。产酶溶杆菌中宁溶霉素的合成主要受到转录因子Clp和第二信使c-di-GMP的调控。其中，Clp可以直接结合在HSAF合成基因簇的启动子上激活其转录，促进HSAF合成，而高浓度的c-di-GMP可以结合Clp并使其与启动子解离，从而抑制HSAF的合成。鸟苷酸环化酶（DGC）和磷酸二脂酶（PDE）是c-di-GMP合成与降解的关键酶，产酶溶杆菌中一些特异的蛋白互作如Clp与LchP（PDE）互作、CdgL与WspR（DGC）互作，构成了该细菌胞内特有的c-di-GMP信号通路来调控宁溶霉素的合成。产酶溶杆菌虽然不能产生抗革兰氏阴性细菌的代谢产物，但利用T4SS，它能够通过细胞间的接触转运毒性效应蛋白，实现对其他革兰氏阴性细菌生长的抑制。同时，产酶溶杆菌还能利用T4SS向土著病原细菌和其他生防细菌体内转运多种非毒性效应蛋白进入，抑制它们的群体感应或激活它们抗菌代谢产物合成，从而建立过去未知的微生物种间互作新方式。产酶溶杆菌独特的生防特征及其背后的调控机制揭示了生防细菌发挥抑菌功能的新途径，为该细菌高效生防菌剂的研发和应用提供了坚实的理论支撑。

Abstract:

Lysobacter enzymogenes is less-studied, but emerging as a powerful biocontrol bacterium producing multiple antimicrobial weapons including lytic enzymes, toxins, secondary metabolites and protein secretion systems. The loss of surface-attached flagellum, production of heat-stable antifungal factor (HSAF, also named as Ningrongmycin) as a novel antifungal antibiotic, and the use of the type IV secretion system (T4SS) rather than the common type VI secretion system (T6SS) to kill competitor bacteria make this species unique. These distinct features set L. enzymogenes apart from well-studied plant beneficial biocontrol agents, such as Bacillus and Pseudomonas. This review describes what takes L. enzymogenes to be a unique biocontrol warrior by focusing to illustrate how the lack of flagellum governs morphological and functional co-adaptability, what adapted signaling transduction pathways are adopted to coordinate the biosynthesis of HSAF, and how to ecologically adapt plant rhizosphere by cell-to-cell interacting with microbiome members via the bacterial-killing T4SS.

Key words: Lysobacter enzymogenes , antimicrobial metabolites , loss of flagella , type IV secretion system

Long Lin, Xiaolong Shao, Yicheng Yang, Aprodisia Kavutu Murero, Limin Wang, Gaoge Xu, Yangyang Zhao, Sen Han, Zhenhe Su, Kangwen Xu, Mingming Yang, Jinxing Liao, Kaihuai Li, Fengquan Liu, Guoliang Qian. 产酶溶杆菌：“一位全副武装的生防战士”[J]. Journal of Integrative Agriculture, 2025, 24(1): 23-35.

Long Lin, Xiaolong Shao, Yicheng Yang, Aprodisia Kavutu Murero, Limin Wang, Gaoge Xu, Yangyang Zhao, Sen Han, Zhenhe Su, Kangwen Xu, Mingming Yang, Jinxing Liao, Kaihuai Li, Fengquan Liu, Guoliang Qian. Lysobacter enzymogenes: A fully armed biocontrol warrior[J]. Journal of Integrative Agriculture, 2025, 24(1): 23-35.

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产酶溶杆菌：“一位全副武装的生防战士”

Lysobacter enzymogenes: A fully armed biocontrol warrior

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