Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch

Abstract Bacillus subtilis, a plant-beneficial bacterial species exhibiting good biocontrol capabilities, has been widely used in agricultural production. The endophytic strain 9407 can efficiently control bacterial fruit blotch (BFB) caused by the gram-negative bacterium Acidovorax citrulli. Howeve...

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Main Authors: Xiaofei Gu, Qingchao Zeng, Yu Wang, Jishun Li, Yu Zhao, Yan Li, Qi Wang
Format: Article
Language:English
Published: BMC 2021-02-01
Series:Phytopathology Research
Subjects:
Online Access:https://doi.org/10.1186/s42483-021-00081-2
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author Xiaofei Gu
Qingchao Zeng
Yu Wang
Jishun Li
Yu Zhao
Yan Li
Qi Wang
author_facet Xiaofei Gu
Qingchao Zeng
Yu Wang
Jishun Li
Yu Zhao
Yan Li
Qi Wang
author_sort Xiaofei Gu
collection DOAJ
description Abstract Bacillus subtilis, a plant-beneficial bacterial species exhibiting good biocontrol capabilities, has been widely used in agricultural production. The endophytic strain 9407 can efficiently control bacterial fruit blotch (BFB) caused by the gram-negative bacterium Acidovorax citrulli. However, the mechanism underlying its biocontrol ability remains poorly understood. Given the genomic diversity of B. subtilis, strain 9407 was sequenced and assembled in this study to determine the genome information associated with its biocontrol traits. A combination of core genome phylogenetic analysis and average nucleotide identity (ANI) analysis demonstrated that the 9407 strain belonged to B. subtilis. Various functional genes related to biocontrol traits, i.e., biofilm formation, motility, pathogen inhibition, plant growth promotion, and induction of systemic resistance, were identified in B. subtilis 9407. Four secondary metabolite biosynthesis gene clusters with antibacterial ability were also found in the B. subtilis 9407 genome, including newly identified subtilosin A, bacilysin, and bacillaene, and the previously reported surfactin. Mutants lacking sboA or bacG, which are defective in synthesizing subtilosin A or bacilysin, showed decreased inhibitory activity against A. citrulli MH21, and the triple mutant with deleted sboA, bacG, and srfAB almost completely lost its inhibitory activity. The biofilm formation and swarming motility of the sboA and bacG mutants also decreased, in turn leading to decreased colonization on melon roots and leaves. Under greenhouse conditions, the biocontrol efficacy of the sboA and bacG mutants against BFB on melon leaves decreased by 21.4 and 32.3%, respectively. Here, we report a new biocontrol pathway of B. subtilis 9407 against BFB, in which subtilosin A and bacilysin contributed to the biocontrol efficacy by improving antibacterial activity and colonization ability of the strain. The comprehensive genomic analysis of B. subtilis 9407 improves our understanding of the biocontrol mechanisms of B. subtilis, providing support for further research of its biocontrol mechanisms and field applications.
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spelling doaj.art-3092420d80214677b1bc6f3b24c02bfc2022-12-21T22:46:45ZengBMCPhytopathology Research2524-41672021-02-013111210.1186/s42483-021-00081-2Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotchXiaofei Gu0Qingchao Zeng1Yu Wang2Jishun Li3Yu Zhao4Yan Li5Qi Wang6Department of Plant Pathology, MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural UniversityBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry UniversityOrdos Plant Protection and Quarantine StationEcology Institute, Qilu University of Technology (Shandong Academy of Sciences)Department of Plant Pathology, MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural UniversityDepartment of Plant Pathology, MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural UniversityDepartment of Plant Pathology, MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural UniversityAbstract Bacillus subtilis, a plant-beneficial bacterial species exhibiting good biocontrol capabilities, has been widely used in agricultural production. The endophytic strain 9407 can efficiently control bacterial fruit blotch (BFB) caused by the gram-negative bacterium Acidovorax citrulli. However, the mechanism underlying its biocontrol ability remains poorly understood. Given the genomic diversity of B. subtilis, strain 9407 was sequenced and assembled in this study to determine the genome information associated with its biocontrol traits. A combination of core genome phylogenetic analysis and average nucleotide identity (ANI) analysis demonstrated that the 9407 strain belonged to B. subtilis. Various functional genes related to biocontrol traits, i.e., biofilm formation, motility, pathogen inhibition, plant growth promotion, and induction of systemic resistance, were identified in B. subtilis 9407. Four secondary metabolite biosynthesis gene clusters with antibacterial ability were also found in the B. subtilis 9407 genome, including newly identified subtilosin A, bacilysin, and bacillaene, and the previously reported surfactin. Mutants lacking sboA or bacG, which are defective in synthesizing subtilosin A or bacilysin, showed decreased inhibitory activity against A. citrulli MH21, and the triple mutant with deleted sboA, bacG, and srfAB almost completely lost its inhibitory activity. The biofilm formation and swarming motility of the sboA and bacG mutants also decreased, in turn leading to decreased colonization on melon roots and leaves. Under greenhouse conditions, the biocontrol efficacy of the sboA and bacG mutants against BFB on melon leaves decreased by 21.4 and 32.3%, respectively. Here, we report a new biocontrol pathway of B. subtilis 9407 against BFB, in which subtilosin A and bacilysin contributed to the biocontrol efficacy by improving antibacterial activity and colonization ability of the strain. The comprehensive genomic analysis of B. subtilis 9407 improves our understanding of the biocontrol mechanisms of B. subtilis, providing support for further research of its biocontrol mechanisms and field applications.https://doi.org/10.1186/s42483-021-00081-2Bacillus subtilisGenomic analysisBiocontrol mechanismBacterial fruit blotchSubtilosin ABacilysin
spellingShingle Xiaofei Gu
Qingchao Zeng
Yu Wang
Jishun Li
Yu Zhao
Yan Li
Qi Wang
Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch
Phytopathology Research
Bacillus subtilis
Genomic analysis
Biocontrol mechanism
Bacterial fruit blotch
Subtilosin A
Bacilysin
title Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch
title_full Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch
title_fullStr Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch
title_full_unstemmed Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch
title_short Comprehensive genomic analysis of Bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch
title_sort comprehensive genomic analysis of bacillus subtilis 9407 reveals its biocontrol potential against bacterial fruit blotch
topic Bacillus subtilis
Genomic analysis
Biocontrol mechanism
Bacterial fruit blotch
Subtilosin A
Bacilysin
url https://doi.org/10.1186/s42483-021-00081-2
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