Effect of nicotine from tobacco root exudates on chemotaxis, growth, biocontrol efficiency, and colonization by Pseudomonas aeruginosa NXHG29

Abstract

Accumulated evidence suggests that root exudates have a major role in mediating plant-microbe interactions in the rhizosphere. Here, we characterized tobacco root exudates (TREs) by GC-MS and nicotine, scopoletin, and octadecane were identified as three main components of TREs. Qualitative and quantitative chemotaxis assays revealed that Pseudomonas aeruginosa NXHG29 with antagonistic activity displayed positive chemotactic responses towards TREs and their three main components (nicotine, scopoletin, octadecane) and its enhanced chemotaxis were induced by these substances in a concentration-dependent manner. Furthermore, following GC-MS and chemotaxis analysis, nicotine was selected as the target for evaluation of the effect on NXHG29 regarding antagonism, growth, root colonization and biocontrol efficiency. Results of in vitro studies showed that nicotine as a sole carbon source could enhance growth of NXHG29 and significantly increased the antagonism of NXHG29. We also demonstrated that nicotine exerted enhancing effects on the colonization ability of NXHG29 on tobacco roots by combining CLSM observations with investigation of population level dynamics by selective dilution plating method. Results from greenhouse experiments suggested nicotine exhibited stimulatory effects on the biocontrol efficiency of NXHG29 against bacterial wilt and black shank on tobacco. The stimulatory effect of nicotine was affected by the concentration and timing of nicotine application and further supported by the results of population level of NXHG29 on tobacco roots. This is the first report on the enhancement effect of nicotine from TREs on an antagonistic bacterium for its root colonization, control of soil-borne pathogens, regarding the chemotaxis and in vitro antagonism and growth.

Whole Genome Sequence of Bacillus velezensis Strain GUMT319: A Potential Biocontrol Agent Against Tobacco Black Shank Disease

“…Qualitative analyses of the freeze-dried tobacco and pepper root exudates were performed by GC-TOF-MS, and 248 peaks ( Supplementary Figure 2 ) were detected, including amino acids, organic acids, and others (data not shown). Here, some organic acids (cinnamic acid, fumaric acid, phthalic acid, benzoic acid, and lauric acid) and nicotine were selected as the targets for evaluation of their roles on B. velezensis GUMT319 ( Zhang et al, 2014 ; Feng et al, 2018 ; Ma et al, 2018 ). Cinnamic acid, fumaric acid, and benzoic acid were detected both in tobacco and pepper root exudates.…”

“…It was found that organic acids were the most represented class of compounds in both plants. Hence, some organic acids (cinnamic acid, fumaric acid, phthalic acid, benzoic acid, and lauric acid) ( Zhang et al, 2014 ; Feng et al, 2018 ) and nicotine ( Ma et al, 2018 ) were selected as targets for the evaluation of their roles on B. velezensis GUMT319. Cinnamic acid, fumaric acid, and benzoic acid were detected both in tobacco and pepper root exudates, phthalic acid and nicotine in tobacco root exudates, and lauric acid only in pepper root exudates.…”

“…Compared with other root-secreted compounds, it was first reported that nicotine in the root exudates of tobacco was a chemoattractant for B. velezensis GUMT319. Previous research shows that nicotine from tobacco root exudates has the ability to enhance chemotaxis, growth, biocontrol efficiency, and colonization by Pseudomonas aeruginosa NXHG29 ( Ma et al, 2018 ). However, we do not know how B. velezensis GUMT319 recognizes nicotine and regulates chemotaxis and root colonization.…”

Plant–Microbiome Crosstalk: Dawning from Composition and Assembly of Microbial Community to Improvement of Disease Resilience in Plants

“…QS is an intercellular communication system, in which particular signal molecules including AHLs mediate bacterial gene expression and bacterial cell concentration [90]. In fact, QS system controls the production of a variety of phenotypes, many of which have been linked to pathogenesis in a variety of economically significant bacterial pathogens, such as Pectobacterium carotovorum, Pseudomonas syringae, Dickeya solani, Ralstonia solanacearum, Erwinia amylovora, and Agrobacterium tumefaciens [91]. In agriculture, interference or interrupting QS is thus an intriguing technique for preventing pathogen infections [92].…”

“…Quorum quenching (QQ), involving the enzymatic destruction of AHL signal molecules, is one of the most well-known QS-interrupting techniques [93]. For example, the QQ activity of Pseudomonas segetis strain P6 reduced soft rot symptoms on potato and carrot caused by D. solani, P. carotovorum, and Pectobacterium atrosepticum [91]. Moreover, plants are also able to disrupt the QS system by producing QS inhibitors, which either degrade QS signals or compete for signal receptors.…”