Please wait a minute...
Journal of Integrative Agriculture  2025, Vol. 24 Issue (1): 23-35    DOI: 10.1016/j.jia.2024.02.021
Review Advanced Online Publication | Current Issue | Archive | Adv Search |
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 Liu2, 7#, Guoliang Qian1#

1 Key Laboratory of Integrated Management of Crop Diseases and Pests/College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China

2 Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing 210014, China

3 Integrated Pest Management Innovation Center of Hebei Province, Plant Protection Institute, Hebei Academy of Agriculture and Forestry Sciences, Baoding 071000, China

4 Marine Agriculture Research Center, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China

5 College of Plant Protection, Northwest A&F University, Yangling 712100, China

6 Hunan Provincial Key Laboratory for Biology and Control of Plant Diseases and Plant Pests, College of Plant Protection, Hunan Agricultural University, Changsha 410128, China

7 Department of Plant Pathology, College of Agriculture, Guizhou University, Guiyang 550025, China

 Highlights 
● The absence of crucial flagellar components results in the flagellum loss in Lysobacter enzymogenes, despite the presence of genes encoding the flagellar type III secretion system responsible for releasing antifungal toxins.
● The production of heat-stable antifungal factor (HSAF, also known as Ningrongmycin) in L. enzymogenes is governed by the key transcription factor Clp and specific c-di-GMP signaling pathways.
● During intercellular contact, L. enzymogenes delivers effectors into cells of ecologically-related bacteria via the type IV secretion system, modulating their physiological functions.
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
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.


Keywords:  Lysobacter enzymogenes       antimicrobial metabolites       loss of flagella       type IV secretion system  
Received: 30 November 2023   Accepted: 29 January 2024
Fund: 
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).

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

Cite this article: 

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. 2025. Lysobacter enzymogenes: A fully armed biocontrol warrior. Journal of Integrative Agriculture, 24(1): 23-35.

Biessy A, Filion M. 2018. Phenazines in plant-beneficial Pseudomonas spp.: Biosynthesis, regulation, function and genomics. Environmental Microbiology, 20, 3905–3917.

Burrows L L. 2012. Pseudomonas aeruginosa twitching motility: Type IV pili in action. Annual Review of Microbiology, 66, 493–520.

Chang Y W, Rettberg L A, Treuner-Lange A, Iwasa J, Sogaard-Andersen L, Jensen G J. 2016. Architecture of the type IVa pilus machine. Science, 351, aad2001.

Chen D M, Huang J G, Yuan L. 2019. A new function of the biocontrol bacterium Lysobacter enzymogenes LE16 in the mineralization of soil organic phosphorus. Plant and Soil, 442, 299–309.

Chen J, Moore W H, Yuen G Y, Kobayashi D, Caswell-Chen E P. 2006. Influence of Lysobacter enzymogenes strain C3 on nematodes. Journal of Nematology, 38, 233–239.

Chen J, Shen D, Odhiambo B O, Xu D, Han S, Chou S H, Qian G. 2018. Two direct gene targets contribute to Clp-dependent regulation of type IV pilus-mediated twitching motility in Lysobacter enzymogenes OH11. Applied Microbiology and Biotechnology, 102, 7509–7519.

Christensen P, Cook F D. 1978. Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio. International Journal of Systematic and Evolutionary Microbiology, 28, 367–393.

Ding Y J, Li Y Y, Li Z Y, Zhang J L, Lu C H, Wang H X, Shen Y M, Du L C. 2016. Alteramide B is a microtubule antagonist of inhibiting. Biochimica et Biophysica Acta (General Subjects), 1860, 2097–2106.

Drenker C, El Mazouar D, Bucker G, Weisshaupt S, Wienke E, Koch E, Kunz S, Reineke A, Rondot Y, Linkies A. 2023. Characterization of a disease-suppressive isolate of Lysobacter enzymogenes with broad antagonistic activity against bacterial, oomycetal and fungal pathogens in different crops. Plants (Basel), 12, 682.

Folman L B, De Klein M J E M, Postma J, van Veen J A. 2004. Production of antifungal compounds by isolate 3.1T8 under different conditions in relation to its efficacy as a biocontrol agent of in cucumber. Biological Control, 31, 145–154.

Folman L B, Postma J, van Veen J A. 2003. Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1T8, a powerful antagonist of fungal diseases of cucumber. Microbiological Research, 158, 107–115.

Fulano A M, Shen D, Kinoshita M, Chou S H, Qian G. 2020a. The Homologous components of flagellar type III protein apparatus have acquired a novel function to control twitching motility in a non-flagellated biocontrol bacterium. Biomolecules, 10, 733.

Fulano A M, Shen D, Zhang E H, Shen X, Chou S H, Minamino T, Puopolo G, Qian G. 2020b. Functional divergence of flagellar type III secretion system: A case study in a non-flagellated, predatory bacterium. Computational and Structural Biotechnology Journal, 18, 3368–3376.

Giesler L J, Yuen G Y. 1998. Evaluation of Stenotrophomonas maltophilia strain C3 for biocontrol of brown patch disease. Crop Protection, 17, 509–513.

Girard L, Hofte M, De Mot R. 2020. Lipopeptide families at the interface between pathogenic and beneficial Pseudomonas-plant interactions. Critical Reviews in Microbiology, 46, 397–419.

Gomez Exposito R, Postma J, Raaijmakers J M, De Bruijn I. 2015. Diversity and activity of Lysobacter species from disease suppressive soils. Frontiers in Microbiology, 6, 1243.

Gottig N, Vranych C V, Sgro G G, Piazza A, Ottado J. 2018. HrpE, the major component of the Xanthomonas type three protein secretion pilus, elicits plant immunity responses. Scientific Reports, 8, 9842.

Haas D, Defago G. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology, 3, 307–319.

Han S, Shen D, Wang Y C, Chou S H, Gomelsky M, Gao Y G, Qian G. 2020. A YajQ-LysR-like, cyclic di-GMP-dependent system regulating biosynthesis of an antifungal antibiotic in a crop-protecting bacterium, Lysobacter enzymogenes. Molecular Plant Pathology, 21, 218–229.

Hou R, Li K, Guo B, Zhao Y, Li C, Tang B, Sun W, Wang B, Chen W, Sheng C, Kan J, Zhao Y, Liu F. 2023. Antifungal compound from the predatory bacterium Lysobacter enzymogenes inhibits a plant pathogenic fungus by targeting the AAA ATPase VpVeb1. Journal of Agricultural and Food Chemistry, 71, 15003–15016.

Hueso-Gil A, Calles B, de Lorenzo V. 2020. The Wsp intermembrane complex mediates metabolic control of the swim-attach decision of Pseudomonas putida. Environmental Microbiology, 22, 3535–3547.

Kilic-Ekici O, Yuen G Y. 2003. Induced resistance as a mechanism of biological control by Lysobacter enzymogenes strain C3. Phytopathology, 93, 1103–1110.

Klein T A, Ahmad S, Whitney J C. 2020. Contact-dependent interbacterial antagonism mediated by protein secretion machines. Trends in Microbiology, 28, 387–400.

Kobayashi D Y, Reedy R M, Palumbo J D, Zhou J M, Yuen G Y. 2005. A clp gene homologue belonging to the Crp gene family globally regulates lytic enzyme production, antimicrobial activity, and biological control activity expressed by Lysobacter enzymogenes strain C3. Applied and Environmental Microbiology, 71, 261–269.

Kobayashi D Y, Yuen G Y. 2005. The role of clp-regulated factors in antagonism against Magnaporthe poae and biological control of summer patch disease of Kentucky bluegrass by Lysobacter enzymogenes C3. Canadian Journal of Microbiology, 51, 719–723.

Kobayashi K. 2021. Diverse LXG toxin and antitoxin systems specifically mediate intraspecies competition in Bacillus subtilis biofilms. Plos Genetics, 17, e1009682.

Lazazzara V, Perazzolli M, Pertot I, Biasioli F, Puopolo G, Cappellin L. 2017. Growth media affect the volatilome and antimicrobial activity against Phytophthora infestans in four Lysobacter type strains. Microbiological Research, 201, 52–62.

Li K, Xu G, Wang B, Wu G, Hou R, Liu F. 2021. The predatory soil bacterium Lysobacter reprograms quorum sensing system to regulate antifungal antibiotic production in a cyclic-di-GMP-independent manner. Communications Biology, 4, 1131.

Li S, Calvo A M, Yuen G Y, Du L, Harris S D. 2009. Induction of cell wall thickening by the antifungal compound dihydromaltophilin disrupts fungal growth and is mediated by sphingolipid biosynthesis. Journal of Eukaryotic Microbiology, 56, 182–187.

Li S, Du L, Yuen G, Harris S D. 2006. Distinct ceramide synthases regulate polarized growth in the filamentous fungus Aspergillus nidulans. Molecular Biology of the Cell, 17, 1218–1227.

Li S, Wu X, Zhang L, Shen Y, Du L. 2017. Activation of a cryptic gene cluster in Lysobacter enzymogenes reveals a module/domain portable mechanism of nonribosomal peptide synthetases in the biosynthesis of pyrrolopyrazines. Organic Letters, 19, 5010–5013.

Li Y, Chen H, Ding Y, Xie Y, Wang H, Cerny R L, Shen Y, Du L. 2014. Iterative assembly of two separate polyketide chains by the same single-module bacterial polyketide synthase in the biosynthesis of HSAF. Angewandte Chemie International Edition, 53, 7524–7530.

Liao J, Li Z, Xiong D, Shen D, Wang L, Lin L, Shao X, Liao L, Li P, Zhang L Q, Wang H H, Qian G. 2023. Quorum quenching by a type IVA secretion system effector. The ISME Journal, 17, 1564–1577.

Lin D, McBride M J. 1996. Development of techniques for the genetic manipulation of the gliding bacteria Lysobacter enzymogenes and Lysobacter brunescens. Canadian Journal of Microbiology, 42, 896–902.

Lin L, Li L, Tao M, Wu Q, Zhou L, Wang B, Wang L, Shao X, Zhong C, Qian G. 2023a. Assembly of an active microbial consortium by engineering compatible combinations containing foreign and native biocontrol bacteria of kiwifruit. Computational and Structural Biotechnology Journal, 21, 3672–3679.

Lin L, Xu K, Shen D, Chou S H, Gomelsky M, Qian G. 2021. Antifungal weapons of Lysobacter, a mighty biocontrol agent. Environmental Microbiology, 23, 5704–5715.

Lin L, Yang Z, Tao M, Shen D, Cui C, Wang P, Wang L, Jing M, Qian G, Shao X. 2023b. Lysobacter enzymogenes prevents Phytophthora infection by inhibiting pathogen growth and eliciting plant immune responses. Frontiers in Plant Science, 14, 1116147.

Lou L, Qian G, Xie Y, Hang J, Chen H, Zaleta-Rivera K, Li Y, Shen Y, Dussault P H, Liu F, Du L. 2011. Biosynthesis of HSAF, a tetramic acid-containing macrolactam from Lysobacter enzymogenes. Journal of the American Chemical Society, 133, 643–645.

Lugtenberg B, Kamilova F. 2009. Plant-growth-promoting rhizobacteria. Annual Review of Microbiology, 63, 541–556.

Manera K, Caro F, Li H, Pei T T, Hersch S J, Mekalanos J J, Dong T G. 2021. Sensing of intracellular Hcp levels controls T6SS expression in Vibrio cholerae. Proceedings of the National Academy of Sciences of the United States of America, 118, e2104813118.

Martinez-Servat S, Pinyol-Escala L, Daura-Pich O, Almazan M, Hernandez I, Lopez-Garcia B, Fernandez C. 2023. Characterization of Lysobacter enzymogenes B25, a potential biological control agent of plant-parasitic nematodes, and its mode of action. AIMS Microbiology, 9, 151–176.

Meziane H, Sluis I V D, Loon L C V, Höfte M, Bakker P A H M. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Molecular Plant Pathology, 6, 177–185.

Miller A L, Li S, Eichhorn C D, Zheng Y, Du L. 2023. Identification and biosynthetic study of the siderophore lysochelin in the biocontrol agent Lysobacter enzymogenes. Journal of Agricultural and Food Chemistry, 71, 7418–7426.

Minamino T. 2014. Protein export through the bacterial flagellar type III export pathway. Biochimica et Biophysica Acta, 1843, 1642–1648.

Molina-Henares M A, Ramos-Gonzalez M I, Daddaoua A, Fernandez-Escamilla A M, Espinosa-Urgel M. 2017. FleQ of Pseudomonas putida KT2440 is a multimeric cyclic diguanylate binding protein that differentially regulates expression of biofilm matrix components. Research in Microbiology, 168, 36–45.

Odhiambo B O, Xu G, Qian G, Liu F. 2017. Evidence of an unidentified extracellular heat-stable factor produced by Lysobacter enzymogenes (OH11) that degrade Fusarium graminearum PH1 hyphae. Current Microbiology, 74, 437–448.

Ongena M, Jacques P. 2008. Bacillus lipopeptides: Versatile weapons for plant disease biocontrol. Trends in Microbiology, 16, 115–125.

Ortiz A, Sansinenea E. 2021. Recent advancements for microorganisms and their natural compounds useful in agriculture. Applied Microbiology and Biotechnology, 105, 891–897.

Palumbo J D, Sullivan R F, Kobayashi D Y. 2003. Molecular characterization and expression in Escherichia coli of three beta-1,3-glucanase genes from Lysobacter enzymogenes strain N4-7. Journal of Bacteriology, 185, 4362–4370.

Palumbo J D, Yuen G Y, Jochum C C, Tatum K, Kobayashi D Y. 2005. Mutagenesis of beta-1,3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward Bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology, 95, 701–707.

Patel N, Hillman B, Kobayashi D. 2010. Characterization of Type IV pilus in the bacterial biocontrol agent strain C3. Phytopathology, 100, S98.

Puopolo G, Tomada S, Pertot I. 2018. The impact of the omics era on the knowledge and use of Lysobacter species to control phytopathogenic micro-organisms. Journal of Applied Microbiology, 124, 15–27.

Qian G L, Hu B S, Jiang Y H, Liu F Q. 2009. Identification and characterization of Lysobacter enzymogenes as a biological control agent against some fungal pathogens. Agricultural Sciences in China, 8, 68–75.

Ren X, Ren S, Xu G, Dou W, Chou S H, Chen Y, Qian G. 2020. Knockout of diguanylate cyclase genes in Lysobacter enzymogenes to improve production of antifungal factor and increase its application in seed coating. Current Microbiology, 77, 1006–1015.

Rittenour W R, Chen M, Cahoon E B, Harris S D. 2011. Control of glucosylceramide production and morphogenesis by the Bar1 ceramide synthase in Fusarium graminearum. PLoS ONE, 6, e19385.

Rizzo D M, Lichtveld M, Mazet J A K, Togami E, Miller S A. 2021. Plant health and its effects on food safety and security in a One Health framework: Four case studies. One Health Outlook, 3, 6.

Ryjenkov D A, Tarutina M, Moskvin O V, Gomelsky M. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: Insights into biochemistry of the GGDEF protein domain. Journal of Bacteriology, 187, 1792–1798.

Sanguankiattichai N, Buscaill P, Preston G M. 2022. How bacteria overcome flagellin pattern recognition in plants. Current Opinion in Plant Biology, 67, 102224.

Savary S, Willocquet L, Pethybridge S J, Esker P, McRoberts N, Nelson A. 2019. The global burden of pathogens and pests on major food crops. Nature Ecology and Evolution, 3, 430–439.

Scharf B E, Hynes M F, Alexandre G M. 2016. Chemotaxis signaling systems in model beneficial plant-bacteria associations. Plant Molecular Biology, 90, 549–559.

Schmidt A J, Ryjenkov D A, Gomelsky M. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: Enzymatically active and inactive EAL domains. Journal of Bacteriology, 187, 4774–4781.

Shen X, Wang B, Yang N, Zhang L, Shen D, Wu H, Dong Y, Niu B, Chou S H, Puopolo G, Fan J, Qian G. 2021. Lysobacter enzymogenes antagonizes soilborne bacteria using the type IV secretion system. Environmental Microbiology, 23, 4673–4688.

Su Z H, Han S, Fu Z Q, Qian G L, Liu F Q. 2018. Heat-stable antifungal factor (HSAF) biosynthesis in Lysobacter enzymogenes is controlled by the interplay of two transcription factors and a diffusible molecule. Applied and Environmental Microbiology, 84, e01754–17.

Syed Ab Rahman S F, Singh E, Pieterse C M J, Schenk P M. 2018. Emerging microbial biocontrol strategies for plant pathogens. Plant Science, 267, 102–111.

Wang B, Zhang Z, Xu F, Yang Z, Li Z, Shen D, Wang L, Wu H, Li T, Yan Q, Wei Q, Shao X, Qian G. 2023. Soil bacterium manipulates antifungal weapons by sensing intracellular type IVA secretion system effectors of a competitor. The ISME Journal, 17, 2232–2246.

Wang P, Chen H, Qian G, Liu F. 2017. LetR is a TetR family transcription factor from Lysobacter controlling antifungal antibiotic biosynthesis. Applied Microbiology and Biotechnology, 101, 3273–3282.

Wang Y, Qian G, Li Y, Wang Y, Wang Y, Wright S, Li Y, Shen Y, Liu F, Du L. 2013. Biosynthetic mechanism for sunscreens of the biocontrol agent Lysobacter enzymogenes. PLoS ONE, 8, e66633.

Wang Y, Zhao Y, Zhang J, Zhao Y, Shen Y, Su Z, Xu G, Du L, Huffman J M, Venturi V, Qian G, Liu F. 2014. Transcriptomic analysis reveals new regulatory roles of Clp signaling in secondary metabolite biosynthesis and surface motility in Lysobacter enzymogenes OH11. Applied Microbiology and Biotechnology, 98, 9009–9020.

Wu Q, Wang B, Shen X, Shen D, Wang B, Guo Q, Li T, Shao X, Qian G. 2021. Unlocking the bacterial contact-dependent antibacterial activity to engineer a biocontrol alliance of two species from natural incompatibility to artificial compatibility. Stress Biology, 1, 19.

Xia J, Chen J, Chen Y, Qian G, Liu F. 2018. Type IV pilus biogenesis genes and their roles in biofilm formation in the biological control agent Lysobacter enzymogenes OH11. Applied Microbiology and Biotechnology, 102, 833–846.

Xie Y, Wright S, Shen Y, Du L. 2012. Bioactive natural products from Lysobacter. Natural Product Reports, 29, 1277–1287.

Xiong D, Yang Z, He X, He W, Shen D, Wang L, Lin L, Murero A, Minamino T, Shao X, Qian G. 2023. Loss of flagella-related genes enables a nonflagellated, fungal-predating bacterium to strengthen the synthesis of an antifungal weapon. Microbiology Spectrum, 11, e0414922.

Xiong W, Guo S, Jousset A, Zhao Q Y, Wu H S, Li R, Kowalchuk G A, Shen Q R. 2017. Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biology and Biochemistry, 114, 238–247.

Xu G, Han S, Huo C, Chin K H, Chou S H, Gomelsky M, Qian G, Liu F. 2018. Signaling specificity in the c-di-GMP-dependent network regulating antibiotic synthesis in Lysobacter. Nucleic Acids Research, 46, 9276–9288.

Xu G, Zhou L, Qian G, Liu F. 2022. Diguanylate cyclase and phosphodiesterase interact to maintain the specificity of cyclic di-GMP signaling in the regulation of antibiotic synthesis in Lysobacter enzymogenes. Applied and Environmental Microbiology, 88, e0189521.

Xu K, Lin L, Shen D, Chou S H, Qian G. 2021a. Clp is a “busy” transcription factor in the bacterial warrior, Lysobacter enzymogenes. Computational and Structural Biotechnology Journal, 19, 3564–3572.

Xu K, Shen D, Han S, Chou S H, Qian G. 2021b. A non-flagellated, predatory soil bacterium reprograms a chemosensory system to control antifungal antibiotic production via cyclic di-GMP signalling. Environmental Microbiology, 23, 878–892.

Xu K, Wang L, Xiong D, Chen H, Tong X, Shao X, Li T, Qian G. 2022. The Wsp chemosensory system modulates c-di-GMP-dependent biofilm formation by integrating DSF quorum sensing through the WspR-RpfG complex in Lysobacter. npj Biofilms and Microbiomes, 8, 97.

Xu L X, Wu P, Wright S J, Du L C, Wei X Y. 2015. Bioactive polycyclic tetramate macrolactams from and their absolute configurations by theoretical ECD calculations. Journal of Natural Products, 78, 1841–1847.

Xu S, Zhang Z, Xie X, Shi Y, Chai A, Fan T, Li B, Li L. 2022. Comparative genomics provides insights into the potential biocontrol mechanism of two Lysobacter enzymogenes strains with distinct antagonistic activities. Frontiers in Microbiology, 13, 966986.

Yang H J, Peng L Y, Li Z M, Huang C Y, Huang J G. 2023. Biocontrol of Lysobacter enzymogenes CQ18 against the tobacco powdery mildew fugus, Erysiphe cichoracearum. Chemical and Biological Technologies in Agriculture, 10, 74.

Yang M, Ren S, Shen D, Yang N, Wang B, Han S, Shen X, Chou S H, Qian G. 2020. An intrinsic mechanism for coordinated production of the contact-dependent and contact-independent weapon systems in a soil bacterium. PLoS Pathogens, 16, e1008967.

Yu F, Zaleta-Rivera K, Zhu X, Huffman J, Millet J C, Harris S D, Yuen G, Li X C, Du L. 2007. Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action. Antimicrobial Agents and Chemotherapy, 51, 64–72.

Yue H, Jiang J, Taylor A J, Leite A L, Dodds E D, Du L. 2021. Outer membrane vesicle-mediated codelivery of the antifungal HSAF metabolites and lytic polysaccharide monooxygenase in the predatory Lysobacter enzymogenes. ACS Chemical Biology, 16, 1079–1089.

Yue H, Miller A L, Khetrapal V, Jayaseker V, Wright S, Du L. 2022. Biosynthesis, regulation, and engineering of natural products from Lysobacter. Natural Product Reports, 39, 842–874.

Yuen G Y, Broderick K C, Jochum C C, Chen C J, Caswell-Chen E P. 2018. Control of cyst nematodes by Lysobacter enzymogenes strain C3 and the role of the antibiotic HSAF in the biological control activity. Biological Control, 117, 158–163.

Yuen G Y, Steadman J R, Lindgren D T, Schaff D, Jochum C. 2001. Bean rust biological control using bacterial agents. Crop Protection, 20, 395–402.

Zhang W, Li Y, Qian G, Wang Y, Chen H, Li Y Z, Liu F, Shen Y, Du L. 2011. Identification and characterization of the anti-methicillin-resistant Staphylococcus aureus WAP-8294A2 biosynthetic gene cluster from Lysobacter enzymogenes OH11. Antimicrobial Agents and Chemotherapy, 55, 5581–5589.

Zhang Z, Yuen G Y. 1999. Biological control of Bipolaris sorokiniana on tall fescue by Stenotrophomonas maltophilia strain C3. Phytopathology, 89, 817–822.

Zhang Z, Yuen G Y. 2000. The role of chitinase production by Stenotrophomonas maltophilia strain C3 in biological control of Bipolaris sorokiniana. Phytopathology, 90, 384–389.

Zhao Y, Cheng C, Jiang T, Xu H, Chen Y, Ma Z, Qian G, Liu F. 2019. Control of wheat Fusarium head blight by heat-stable antifungal factor (HSAF) from Lysobacter enzymogenes. Plant Disease, 103, 1286–1292.

Zhao Y, Qian G, Chen Y, Du L, Liu F. 2017. Transcriptional and antagonistic responses of biocontrol strain Lysobacter enzymogenes OH11 to the plant pathogenic oomycete Pythium aphanidermatum. Frontiers in Microbiology, 8, 1025.

Zhu J, Chen Y, Du L. 2022. Production of new WAP-8294a cyclodepsipeptides by the biological control agent Lysobacter enzymogenes OH11. Frontiers of Agricultural Science and Engineering, 9, 120–132.

Zhu X, Yu L, Zhang M, Xu Z, Yao Z, Wu Q, Du X, Li J. 2018. Design, synthesis and biological activity of hydroxybenzoic acid ester conjugates of phenazine-1-carboxylic acid. Chemistry Central Journal, 12, 111.

No related articles found!
No Suggested Reading articles found!