枯草芽孢杆菌生物膜在青枯病生防中的功能研究及Cyclic-di-GMP信号通路初探
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摘要
枯草芽孢杆菌与其他芽孢杆菌属菌株是农业上生防农业病虫害的重要生防菌之一,但其具体生防机理尚未清晰。枯草芽孢杆菌生防植物病害的主效基因是什么?枯草芽孢杆菌生防菌施用后,以什么细胞形态存在于植物根围区?枯草芽孢杆菌如何调控移动相关基因的表达,游动至植物根围?枯草芽孢杆菌与寄主植物直接是否存在信号交流?如若存在信号交流,那么该途径中的信号分子是什么?枯草芽孢杆菌如何接受来自寄主植物的信号分子并调控生防相关基因的表达?等等,这些关于枯草芽孢杆菌生防机理深层次问题的解决,将能更好更有效使用以枯草芽孢杆菌为主要成分的生物农药,推动枯草芽孢杆菌的产业化。
本研究以生防枯草芽孢杆菌防治番茄青枯病为模型,系统研究了枯草芽孢杆菌生防番茄青枯病的机理,发现生物膜形成能力和其抗生物质(主要为表面活性素)在生防青枯病中起主效作用。番茄根系分泌物通过激活枯草芽孢杆菌组氨酸激酶KinD,诱导生物膜的形成。研究还首次报道枯草芽孢杆菌C-di-GMP信号途径调控细胞移动性和生物膜形成,为研究C-di-GMP途径在枯草芽孢杆菌与寄主植物互作过程的信号交流奠定基础。
1.生防枯草芽孢杆菌生物膜、拮抗能力与防治番茄青枯病相关性研究
本试验以生防枯草芽孢杆菌防治番茄青枯病为模型,系统研究了枯草芽孢杆菌生物膜形成能力和其抗生物质(主要为表面活性素)在其生防青枯病中的作用。首先,从自然界根围土中分离筛选得到60株芽孢杆菌菌株,通过16S rDNA测序鉴定其中20株为枯草芽孢杆菌。通过温室防治青枯病试验选取其中防效高于50%的6菌株进行后续生防机理研究。野生型菌株都能形成生物膜,试验构建了生物膜增强和减弱突变体并比较突变体温室生防青枯病效果。结果表明,枯草芽孢杆菌生物膜能增加生防菌在根围的定殖能力,其生物膜形成能力与生防活性呈正相关。抗生物质也是生防枯草芽孢杆菌的生防机理之一。本研究构建了不同抗生基因的突变体,通过平板拮抗试验和温室防病试验发现表面活性剂在抑制青枯菌过程中起重要作用。本研究结果表明,生物膜形成能力和表面活性剂的产生能力是生防枯草芽孢杆菌防治番茄青枯病的重要机理。研究中建立的番茄-枯草芽孢杆菌体系为研究生防菌-寄主植物互作提供基础。
2.枯草芽孢杆菌组氨酸激酶KinD在寄主植物-枯草芽孢杆菌信号交流过程中功能研究
生防枯草芽孢杆菌能够在植物根部及根围形成生物膜并在防病促生过程中起着重要作用。但是,对于枯草芽孢杆菌与寄主植物这种友好的互作过程中的诸多细节报道较少。在互作过程中,枯草芽孢杆菌如何移动至根表并定殖?寄主植物释放的信号分子是什么?枯草芽孢杆菌如何接受来自植物的信号分子并启动生物膜相关基因的表达继而在根表形成生物膜保护寄主免受病原物的侵染?本研究通过建立一种基于无菌培养番茄植株与枯草芽孢杆菌共培养的互作体系来研究两者之间的互作过程,研究结果发现枯草芽孢杆菌通过跨膜的组氨酸激酶KinD接受植物释放的信号分子,并通过构建氨基酸点突变体,发现KinD蛋白结构中CACHE功能域为信号分子的结合位点。番茄的根系分泌物能够诱导Bacillus subtilis生物膜基因和KinD报道基因sdp的表达。通过分离鉴定根系分泌物,并以KinD报道基因PsdpA-lux活性为筛选指标,发现根系分泌物中含有1种以上的活性物质能够增加PsdpA-lux活性,其中L-苹果酸(L-Malic Acid)分子能够通过增强KinD的活性,并增加生物膜的形成。
3.枯草芽孢杆菌C-di-GMP信号通路基因鉴定及其机制分析
C-di-GMP分子广泛存在于细菌中,作为细菌的第二信使分子,其参与调节细菌游动性、生物膜形成、寄主表面定殖能力、致病性及细胞间信号交流等多种生理过程。已报道的关于C-di-GMP分子的信号通路研究主要集中于革兰氏阴性细菌,而革兰氏阳性细菌的报道甚少。本研究首次对革兰氏阳性细菌模式菌枯草芽孢杆菌C-di-GMP信号通路的基因进行分析,并初步探明C-di-GMP信号通路在枯草芽孢杆菌移动性及生物膜形成过程中的作用。试验结果表明,受SpoOA负调控的YuxH蛋白为磷酸二酯酶能够降解细胞体内的C-di-GMP分子。C-di-GMP分子受体蛋白YpfA与C-di-GMP分子结合后发生构象变化并直接与细菌鞭毛动力蛋白MotA互作来调控细胞的游动性。C-di-GMP信号通路直接或间接地影响枯草芽孢杆菌生物膜的形成及降解过程。
4.总结
本研究的主要研究结果与创新点如下：1.从自然界中筛选得到的野生型枯草芽孢杆菌都能形成生物膜,且在各菌株中生物膜形成主要途径是保守的；2.构建了枯草芽孢杆菌-番茄的互作体系,通过比较野生型菌株及对应生物膜突变体的生防青枯病效果,首次报告枯草芽孢杆菌生物膜形成能力与生防效果呈正相关关系；3.首次证明枯草芽孢杆菌的跨膜激酶KinD能够接受植物根系分泌物中的信号分子后激活生物膜形成途径在根表形成生物膜。通过分离鉴定根系分泌物发现,L-苹果酸能够激活KinD激酶；4.首次报道革兰氏阳性细菌枯草芽孢杆菌的C-di-GMP信号通路调控细胞移动性和生物膜形成能力。
Bacillus subtilis and other Bacilli have long been used as biological control agents (BCAs) against plant bacterial diseases. The exact mechanisms for plant biocontrol have not been clearly addressed. There are too many questions needed to address in this field. For example, what are major genes involved in biocontrol efficacy against plant diseases in B. subtilis? Which kind of cell morphology exists in the rhizosphere after application? How do B. subtilis cells move towards plant roots and colonizate on the root surface? Is there a signaling transduction pathway between B. subtilis and plants during the biocontrol? If there is a signal pathway, what are the signaling molecules, and how does B. subtilis or plant recognize the signal and regulate genes expression? It will be beneficial for deeply investigating the B. subtilis biocontrol mechanism and accelerating the commercial procedure of B. subtilis biopesticide.
In this study, we established the B. subtilis-tomato interaction system to gain a better insight into B. subtilis biocontrol mechanism. We showed that in those wild strains, both biofilm formation and production of surfactin, an antimicrobial agent, were necessary for plant biocontrol but neither one was sufficient. B. subtilis kinase KinD can recognize the signaling molecules from tomato root exudates, then active the biofilm formation. We also present the function of C-di-GMP signaling pathway in gram-positive bacterium B. subtilis. C-di-GMP controlled the motility and biofilm formation in B. subtilis.
1. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation and surfactin
Our goal in this study is to first isolate spore-forming B. subtilis wild strains from natural environments that exhibit high biocontrol efficacy. And second, we hope to investigate the molecular mechanisms of plant biocontrol in those wild strains. We screened a total of sixty distinct isolates collected from various locations countrywide and obtained six wild strains of B. subtilis that demonstrated above50%biocontrol efficacy on tomato plants against the plant pathogen Ralstonia solanacearum under greenhouse conditions. These wild strains were able to form robust biofilms both in defined media and on tomato plant roots, and exhibited strong antagonistic activities against various plant pathogens in plate assays. We further showed that in those wild strains, both biofilm formation and production of surfactin, an antimicrobial agent, were necessary for plant biocontrol but neither one was sufficient. Loss of either feature due to genetic mutations resulted in a substantial decrease in biocontrol efficacy. Biofilm formation and surfactin production may act synergistically to enhance biocontrol efficacy. In addition, we showed that biofilm formation strongly promoted colonization of B. subtilis cells to tomato root surfaces, during which the biofilm matrix may function as an adhesion. Finally, we have established a model system for studies of B. subtilis-tomato plant interactions at molecular levels.
2. A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants
The soil bacterium Bacillus subtilis is widely used in agriculture as a biocontrol agent able to protect plants from a variety of pathogens. Protection is thought to involve the formation of bacterial communities-biofilms-on the roots of the plants. Here we used confocal microscopy to visualize biofilms on the surface of the roots of tomato seedlings and demonstrated that biofilm formation requires genes governing the production of the extracellular matrix that holds cells together. We further show that biofilm formation was dependent on the sensor histidine kinase KinD and in particular on an extracellular CACHE domain implicated in small molecule sensing. Finally, we report that exudates of tomato roots strongly stimulated biofilm formation ex planta and that an abundant small molecule in the exudates, L-malic acid, was able to stimulate biofilm formation at high concentrations in a manner that depended on the KinD CACHE domain. We propose that small signaling molecules released by the roots of tomato plants are directly or indirectly recognized by KinD, triggering biofilm formation.
3. Evidence for cyclic di-GMP-mediated signaling in Bacillus subtilis
Cyclic-di-GMP (C-di-GMP) is a second messenger that regulates diverse cellular processes in bacteria, including motility, biofilm formation, cell-cell signaling, and host colonization. Studies of C-di-GMP signaling have chiefly focused on gram-negative bacteria. Here we investigated C-di-GMP signaling in the gram-positive bacterium Bacillus subtilis by constructing deletion mutations for genes predicted to be involved in the synthesis, breakdown, or response to the second messenger. We found that a putative C-di-GMP degrading phosphodiesterase YuxH and a putative C-di-GMP receptor YpfA had a strong influence on motility and that these effects depended on sequences similar to canonical EAL and RxxxR---D/NxSxxG motifs, respectively. Evidence indicates that YpfA inhibits motility by interacting with the flagellar motor protein MotA and that yuxH is under the negative control of the master regulator SpoOA-P. Based on these findings, we propose that YpfA inhibits motility in response to rising levels of c-di-GMP during entry into stationary phase due to the down regulation of yuxH by SpoOA-P. We also present evidence that YpfA has a mild influence on biofilm formation. In toto, our results demonstrate the existence of a functional C-di-GMP signaling system in B. subtilis that directly inhibits motility and directly or indirectly influences biofilm formation.
本研究以生防枯草芽孢杆菌防治番茄青枯病为模型,系统研究了枯草芽孢杆菌生防番茄青枯病的机理,发现生物膜形成能力和其抗生物质(主要为表面活性素)在生防青枯病中起主效作用。番茄根系分泌物通过激活枯草芽孢杆菌组氨酸激酶KinD,诱导生物膜的形成。研究还首次报道枯草芽孢杆菌C-di-GMP信号途径调控细胞移动性和生物膜形成,为研究C-di-GMP途径在枯草芽孢杆菌与寄主植物互作过程的信号交流奠定基础。
1.生防枯草芽孢杆菌生物膜、拮抗能力与防治番茄青枯病相关性研究
本试验以生防枯草芽孢杆菌防治番茄青枯病为模型,系统研究了枯草芽孢杆菌生物膜形成能力和其抗生物质(主要为表面活性素)在其生防青枯病中的作用。首先,从自然界根围土中分离筛选得到60株芽孢杆菌菌株,通过16S rDNA测序鉴定其中20株为枯草芽孢杆菌。通过温室防治青枯病试验选取其中防效高于50%的6菌株进行后续生防机理研究。野生型菌株都能形成生物膜,试验构建了生物膜增强和减弱突变体并比较突变体温室生防青枯病效果。结果表明,枯草芽孢杆菌生物膜能增加生防菌在根围的定殖能力,其生物膜形成能力与生防活性呈正相关。抗生物质也是生防枯草芽孢杆菌的生防机理之一。本研究构建了不同抗生基因的突变体,通过平板拮抗试验和温室防病试验发现表面活性剂在抑制青枯菌过程中起重要作用。本研究结果表明,生物膜形成能力和表面活性剂的产生能力是生防枯草芽孢杆菌防治番茄青枯病的重要机理。研究中建立的番茄-枯草芽孢杆菌体系为研究生防菌-寄主植物互作提供基础。
2.枯草芽孢杆菌组氨酸激酶KinD在寄主植物-枯草芽孢杆菌信号交流过程中功能研究
生防枯草芽孢杆菌能够在植物根部及根围形成生物膜并在防病促生过程中起着重要作用。但是,对于枯草芽孢杆菌与寄主植物这种友好的互作过程中的诸多细节报道较少。在互作过程中,枯草芽孢杆菌如何移动至根表并定殖?寄主植物释放的信号分子是什么?枯草芽孢杆菌如何接受来自植物的信号分子并启动生物膜相关基因的表达继而在根表形成生物膜保护寄主免受病原物的侵染?本研究通过建立一种基于无菌培养番茄植株与枯草芽孢杆菌共培养的互作体系来研究两者之间的互作过程,研究结果发现枯草芽孢杆菌通过跨膜的组氨酸激酶KinD接受植物释放的信号分子,并通过构建氨基酸点突变体,发现KinD蛋白结构中CACHE功能域为信号分子的结合位点。番茄的根系分泌物能够诱导Bacillus subtilis生物膜基因和KinD报道基因sdp的表达。通过分离鉴定根系分泌物,并以KinD报道基因PsdpA-lux活性为筛选指标,发现根系分泌物中含有1种以上的活性物质能够增加PsdpA-lux活性,其中L-苹果酸(L-Malic Acid)分子能够通过增强KinD的活性,并增加生物膜的形成。
3.枯草芽孢杆菌C-di-GMP信号通路基因鉴定及其机制分析
C-di-GMP分子广泛存在于细菌中,作为细菌的第二信使分子,其参与调节细菌游动性、生物膜形成、寄主表面定殖能力、致病性及细胞间信号交流等多种生理过程。已报道的关于C-di-GMP分子的信号通路研究主要集中于革兰氏阴性细菌,而革兰氏阳性细菌的报道甚少。本研究首次对革兰氏阳性细菌模式菌枯草芽孢杆菌C-di-GMP信号通路的基因进行分析,并初步探明C-di-GMP信号通路在枯草芽孢杆菌移动性及生物膜形成过程中的作用。试验结果表明,受SpoOA负调控的YuxH蛋白为磷酸二酯酶能够降解细胞体内的C-di-GMP分子。C-di-GMP分子受体蛋白YpfA与C-di-GMP分子结合后发生构象变化并直接与细菌鞭毛动力蛋白MotA互作来调控细胞的游动性。C-di-GMP信号通路直接或间接地影响枯草芽孢杆菌生物膜的形成及降解过程。
4.总结
本研究的主要研究结果与创新点如下：1.从自然界中筛选得到的野生型枯草芽孢杆菌都能形成生物膜,且在各菌株中生物膜形成主要途径是保守的；2.构建了枯草芽孢杆菌-番茄的互作体系,通过比较野生型菌株及对应生物膜突变体的生防青枯病效果,首次报告枯草芽孢杆菌生物膜形成能力与生防效果呈正相关关系；3.首次证明枯草芽孢杆菌的跨膜激酶KinD能够接受植物根系分泌物中的信号分子后激活生物膜形成途径在根表形成生物膜。通过分离鉴定根系分泌物发现,L-苹果酸能够激活KinD激酶；4.首次报道革兰氏阳性细菌枯草芽孢杆菌的C-di-GMP信号通路调控细胞移动性和生物膜形成能力。
Bacillus subtilis and other Bacilli have long been used as biological control agents (BCAs) against plant bacterial diseases. The exact mechanisms for plant biocontrol have not been clearly addressed. There are too many questions needed to address in this field. For example, what are major genes involved in biocontrol efficacy against plant diseases in B. subtilis? Which kind of cell morphology exists in the rhizosphere after application? How do B. subtilis cells move towards plant roots and colonizate on the root surface? Is there a signaling transduction pathway between B. subtilis and plants during the biocontrol? If there is a signal pathway, what are the signaling molecules, and how does B. subtilis or plant recognize the signal and regulate genes expression? It will be beneficial for deeply investigating the B. subtilis biocontrol mechanism and accelerating the commercial procedure of B. subtilis biopesticide.
In this study, we established the B. subtilis-tomato interaction system to gain a better insight into B. subtilis biocontrol mechanism. We showed that in those wild strains, both biofilm formation and production of surfactin, an antimicrobial agent, were necessary for plant biocontrol but neither one was sufficient. B. subtilis kinase KinD can recognize the signaling molecules from tomato root exudates, then active the biofilm formation. We also present the function of C-di-GMP signaling pathway in gram-positive bacterium B. subtilis. C-di-GMP controlled the motility and biofilm formation in B. subtilis.
1. Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation and surfactin
Our goal in this study is to first isolate spore-forming B. subtilis wild strains from natural environments that exhibit high biocontrol efficacy. And second, we hope to investigate the molecular mechanisms of plant biocontrol in those wild strains. We screened a total of sixty distinct isolates collected from various locations countrywide and obtained six wild strains of B. subtilis that demonstrated above50%biocontrol efficacy on tomato plants against the plant pathogen Ralstonia solanacearum under greenhouse conditions. These wild strains were able to form robust biofilms both in defined media and on tomato plant roots, and exhibited strong antagonistic activities against various plant pathogens in plate assays. We further showed that in those wild strains, both biofilm formation and production of surfactin, an antimicrobial agent, were necessary for plant biocontrol but neither one was sufficient. Loss of either feature due to genetic mutations resulted in a substantial decrease in biocontrol efficacy. Biofilm formation and surfactin production may act synergistically to enhance biocontrol efficacy. In addition, we showed that biofilm formation strongly promoted colonization of B. subtilis cells to tomato root surfaces, during which the biofilm matrix may function as an adhesion. Finally, we have established a model system for studies of B. subtilis-tomato plant interactions at molecular levels.
2. A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants
The soil bacterium Bacillus subtilis is widely used in agriculture as a biocontrol agent able to protect plants from a variety of pathogens. Protection is thought to involve the formation of bacterial communities-biofilms-on the roots of the plants. Here we used confocal microscopy to visualize biofilms on the surface of the roots of tomato seedlings and demonstrated that biofilm formation requires genes governing the production of the extracellular matrix that holds cells together. We further show that biofilm formation was dependent on the sensor histidine kinase KinD and in particular on an extracellular CACHE domain implicated in small molecule sensing. Finally, we report that exudates of tomato roots strongly stimulated biofilm formation ex planta and that an abundant small molecule in the exudates, L-malic acid, was able to stimulate biofilm formation at high concentrations in a manner that depended on the KinD CACHE domain. We propose that small signaling molecules released by the roots of tomato plants are directly or indirectly recognized by KinD, triggering biofilm formation.
3. Evidence for cyclic di-GMP-mediated signaling in Bacillus subtilis
Cyclic-di-GMP (C-di-GMP) is a second messenger that regulates diverse cellular processes in bacteria, including motility, biofilm formation, cell-cell signaling, and host colonization. Studies of C-di-GMP signaling have chiefly focused on gram-negative bacteria. Here we investigated C-di-GMP signaling in the gram-positive bacterium Bacillus subtilis by constructing deletion mutations for genes predicted to be involved in the synthesis, breakdown, or response to the second messenger. We found that a putative C-di-GMP degrading phosphodiesterase YuxH and a putative C-di-GMP receptor YpfA had a strong influence on motility and that these effects depended on sequences similar to canonical EAL and RxxxR---D/NxSxxG motifs, respectively. Evidence indicates that YpfA inhibits motility by interacting with the flagellar motor protein MotA and that yuxH is under the negative control of the master regulator SpoOA-P. Based on these findings, we propose that YpfA inhibits motility in response to rising levels of c-di-GMP during entry into stationary phase due to the down regulation of yuxH by SpoOA-P. We also present evidence that YpfA has a mild influence on biofilm formation. In toto, our results demonstrate the existence of a functional C-di-GMP signaling system in B. subtilis that directly inhibits motility and directly or indirectly influences biofilm formation.
引文
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