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Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities

Ralstonia solanacearum, the causative agent of bacterial wilt disease, has been a major threat to tobacco production globally. Several control methods have failed. Thus, it is imperative to find effective management for this disease. The biocontrol agent Bacillus amyloliquefaciens WS-10 displayed a...

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Autores principales: Ahmed, Waqar, Dai, Zhenlin, Zhang, Jinhao, Li, Shichen, Ahmed, Ayesha, Munir, Shahzad, Liu, Qi, Tan, Yujiao, Ji, Guanghai, Zhao, Zhengxiong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9430121/
https://www.ncbi.nlm.nih.gov/pubmed/35913211
http://dx.doi.org/10.1128/spectrum.01471-22
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author Ahmed, Waqar
Dai, Zhenlin
Zhang, Jinhao
Li, Shichen
Ahmed, Ayesha
Munir, Shahzad
Liu, Qi
Tan, Yujiao
Ji, Guanghai
Zhao, Zhengxiong
author_facet Ahmed, Waqar
Dai, Zhenlin
Zhang, Jinhao
Li, Shichen
Ahmed, Ayesha
Munir, Shahzad
Liu, Qi
Tan, Yujiao
Ji, Guanghai
Zhao, Zhengxiong
author_sort Ahmed, Waqar
collection PubMed
description Ralstonia solanacearum, the causative agent of bacterial wilt disease, has been a major threat to tobacco production globally. Several control methods have failed. Thus, it is imperative to find effective management for this disease. The biocontrol agent Bacillus amyloliquefaciens WS-10 displayed a significant control effect due to biofilm formation, and secretion of hydrolytic enzymes and exopolysaccharides. In addition, strain WS-10 can produce antimicrobial compounds, which was confirmed by the presence of genes encoding antimicrobial lipopeptides (fengycin, iturin, surfactin, and bacillomycinD) and polyketides (difficidin, bacilysin, bacillibactin, and bacillaene). Strain WS-10 successfully colonized tobacco plant roots and rhizosphere soil and suppressed the incidence of bacterial wilt disease up to 72.02% by reducing the R. solanacearum population dynamic in rhizosphere soil. Plant-microbe interaction was considered a key driver of disease outcome. To further explore the impact of strain WS-10 on rhizosphere microbial communities, V3-V4 and ITS1 variable regions of 16S and ITS rRNA were amplified, respectively. Results revealed that strain WS-10 influences the rhizosphere microbial communities and dramatically changed the diversity and composition of rhizosphere microbial communities. Interestingly, the relative abundance of genus Ralstonia significantly decreased when treated with strain WS-10. A complex microbial co-occurrence network was present in a diseased state, and the introduction of strain WS-10 significantly changed the structure of rhizosphere microbiota. This study suggests that strain WS-10 can be used as a novel biocontrol agent to attain sustainability in disease management due to its intense antibacterial activity, efficient colonization in the host plant, and ability to transform the microbial community structure toward a healthy state. IMPORTANCE The plant rhizosphere acts as the first line of defense against the invasion of pathogens. The perturbation in the rhizosphere microbiome is directly related to plant health and disease development. The introduction of beneficial microorganisms in the soil shifted the rhizosphere microbiome, induced resistance in plants, and suppressed the incidence of soilborne disease. Bacillus sp. is widely used as a biocontrol agent against soilborne diseases due to its ability to produce broad-spectrum antimicrobial compounds and colonization with the host plant. In our study, we found that the application of native Bacillus amyloliquefaciens WS-10 significantly suppressed the incidence of tobacco bacterial wilt disease by shifting the rhizosphere microbiome and reducing the interaction between rhizosphere microorganisms and bacterial wilt pathogen.
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spelling pubmed-94301212022-09-01 Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities Ahmed, Waqar Dai, Zhenlin Zhang, Jinhao Li, Shichen Ahmed, Ayesha Munir, Shahzad Liu, Qi Tan, Yujiao Ji, Guanghai Zhao, Zhengxiong Microbiol Spectr Research Article Ralstonia solanacearum, the causative agent of bacterial wilt disease, has been a major threat to tobacco production globally. Several control methods have failed. Thus, it is imperative to find effective management for this disease. The biocontrol agent Bacillus amyloliquefaciens WS-10 displayed a significant control effect due to biofilm formation, and secretion of hydrolytic enzymes and exopolysaccharides. In addition, strain WS-10 can produce antimicrobial compounds, which was confirmed by the presence of genes encoding antimicrobial lipopeptides (fengycin, iturin, surfactin, and bacillomycinD) and polyketides (difficidin, bacilysin, bacillibactin, and bacillaene). Strain WS-10 successfully colonized tobacco plant roots and rhizosphere soil and suppressed the incidence of bacterial wilt disease up to 72.02% by reducing the R. solanacearum population dynamic in rhizosphere soil. Plant-microbe interaction was considered a key driver of disease outcome. To further explore the impact of strain WS-10 on rhizosphere microbial communities, V3-V4 and ITS1 variable regions of 16S and ITS rRNA were amplified, respectively. Results revealed that strain WS-10 influences the rhizosphere microbial communities and dramatically changed the diversity and composition of rhizosphere microbial communities. Interestingly, the relative abundance of genus Ralstonia significantly decreased when treated with strain WS-10. A complex microbial co-occurrence network was present in a diseased state, and the introduction of strain WS-10 significantly changed the structure of rhizosphere microbiota. This study suggests that strain WS-10 can be used as a novel biocontrol agent to attain sustainability in disease management due to its intense antibacterial activity, efficient colonization in the host plant, and ability to transform the microbial community structure toward a healthy state. IMPORTANCE The plant rhizosphere acts as the first line of defense against the invasion of pathogens. The perturbation in the rhizosphere microbiome is directly related to plant health and disease development. The introduction of beneficial microorganisms in the soil shifted the rhizosphere microbiome, induced resistance in plants, and suppressed the incidence of soilborne disease. Bacillus sp. is widely used as a biocontrol agent against soilborne diseases due to its ability to produce broad-spectrum antimicrobial compounds and colonization with the host plant. In our study, we found that the application of native Bacillus amyloliquefaciens WS-10 significantly suppressed the incidence of tobacco bacterial wilt disease by shifting the rhizosphere microbiome and reducing the interaction between rhizosphere microorganisms and bacterial wilt pathogen. American Society for Microbiology 2022-08-01 /pmc/articles/PMC9430121/ /pubmed/35913211 http://dx.doi.org/10.1128/spectrum.01471-22 Text en Copyright © 2022 Ahmed et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Ahmed, Waqar
Dai, Zhenlin
Zhang, Jinhao
Li, Shichen
Ahmed, Ayesha
Munir, Shahzad
Liu, Qi
Tan, Yujiao
Ji, Guanghai
Zhao, Zhengxiong
Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities
title Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities
title_full Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities
title_fullStr Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities
title_full_unstemmed Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities
title_short Plant-Microbe Interaction: Mining the Impact of Native Bacillus amyloliquefaciens WS-10 on Tobacco Bacterial Wilt Disease and Rhizosphere Microbial Communities
title_sort plant-microbe interaction: mining the impact of native bacillus amyloliquefaciens ws-10 on tobacco bacterial wilt disease and rhizosphere microbial communities
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9430121/
https://www.ncbi.nlm.nih.gov/pubmed/35913211
http://dx.doi.org/10.1128/spectrum.01471-22
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