Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanism

Many Bacillus species are essential antibacterial agents, but their antibiosis potential still needs to be elucidated to its full extent. Here, we isolated a soil bacterium, BP9, which has significant antibiosis activity against fungal and bacterial pathogens. BP9 improved the growth of wheat seedli...

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Main Authors: Muhammad Asif, Zhang Li-Qun, Qingchao Zeng, Muhammad Atiq, Khalil Ahmad, Aqil Tariq, Nadhir Al-Ansari, Jochen Blom, Linda Fenske, Hissah Abdulrahman Alodaini, Ashraf Atef Hatamleh
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:Computational and Structural Biotechnology Journal
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Online Access:http://www.sciencedirect.com/science/article/pii/S2001037023003550
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author Muhammad Asif
Zhang Li-Qun
Qingchao Zeng
Muhammad Atiq
Khalil Ahmad
Aqil Tariq
Nadhir Al-Ansari
Jochen Blom
Linda Fenske
Hissah Abdulrahman Alodaini
Ashraf Atef Hatamleh
author_facet Muhammad Asif
Zhang Li-Qun
Qingchao Zeng
Muhammad Atiq
Khalil Ahmad
Aqil Tariq
Nadhir Al-Ansari
Jochen Blom
Linda Fenske
Hissah Abdulrahman Alodaini
Ashraf Atef Hatamleh
author_sort Muhammad Asif
collection DOAJ
description Many Bacillus species are essential antibacterial agents, but their antibiosis potential still needs to be elucidated to its full extent. Here, we isolated a soil bacterium, BP9, which has significant antibiosis activity against fungal and bacterial pathogens. BP9 improved the growth of wheat seedlings via active colonization and demonstrated effective biofilm and swarming activity. BP9 sequenced genome contains 4282 genes with a mean G-C content of 45.94% of the whole genome. A single copy concatenated 802 core genes of 28 genomes, and their calculated average nucleotide identity (ANI) discriminated the strain BP9 from Bacillus licheniformis and classified it as Bacillus paralicheniformis. Furthermore, a comparative pan-genome analysis of 40 B. paralicheniformis strains suggested that the genetic repertoire of BP9 belongs to open-type genome species. A comparative analysis of a pan-genome dataset using the Kyoto Encyclopedia of Genes and Genomes (KEGG) and Cluster of Orthologous Gene groups (COG) revealed the diversity of secondary metabolic pathways, where BP9 distinguishes itself by exhibiting a greater prevalence of loci associated with the metabolism and transportation of organic and inorganic substances, carbohydrate and amino acid for effective inhabitation in diverse environments. The primary secondary metabolites and their genes involved in synthesizing bacillibactin, fencing, bacitracin, and lantibiotics were identified as acquired through a recent Horizontal gene transfer (HGT) event, which contributes to a significant part of the strain`s antimicrobial potential. Finally, we report some genes essential for plant-host interaction identified in BP9, which reduce spore germination and virulence of multiple fungal and bacterial species. The effective colonization, diverse predicted metabolic pathways and secondary metabolites (antibiotics) suggest testing the suitability of strain BP9 as a potential bio-preparation in agricultural fields.
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spelling doaj.art-76d4cadebf3e447db4533d5c22cd1b0f2023-12-21T07:32:15ZengElsevierComputational and Structural Biotechnology Journal2001-03702023-01-012146474662Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanismMuhammad Asif0Zhang Li-Qun1Qingchao Zeng2Muhammad Atiq3Khalil Ahmad4Aqil Tariq5Nadhir Al-Ansari6Jochen Blom7Linda Fenske8Hissah Abdulrahman Alodaini9Ashraf Atef Hatamleh10Department of Plant Pathology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing 100193, ChinaDepartment of Plant Pathology and MOA Key Lab of Pest Monitoring and Green Management, College of Plant Protection, China Agricultural University, Beijing 100193, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, ChinaDepartment of Plant Pathology, University of Agriculture, Faisalabad 38000, PakistanSchool of Ecological and Environmental Sciences, East China Normal University, Shanghai 200241, ChinaDepartment of Wildlife, Fisheries, and Aquaculture, College of Forest Resources, Mississippi State, University, MS 39762-9690, USA; Corresponding authors.Lulea University of Technology, Lulea 97187, Sweden; Corresponding authors.Bioinformatics and Systems Biology, Justus Liebig University, Giessen 35392, GermanyBioinformatics and Systems Biology, Justus Liebig University, Giessen 35392, GermanyDepartment of Botany and Microbiology, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi ArabiaDepartment of Botany and Microbiology, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi ArabiaMany Bacillus species are essential antibacterial agents, but their antibiosis potential still needs to be elucidated to its full extent. Here, we isolated a soil bacterium, BP9, which has significant antibiosis activity against fungal and bacterial pathogens. BP9 improved the growth of wheat seedlings via active colonization and demonstrated effective biofilm and swarming activity. BP9 sequenced genome contains 4282 genes with a mean G-C content of 45.94% of the whole genome. A single copy concatenated 802 core genes of 28 genomes, and their calculated average nucleotide identity (ANI) discriminated the strain BP9 from Bacillus licheniformis and classified it as Bacillus paralicheniformis. Furthermore, a comparative pan-genome analysis of 40 B. paralicheniformis strains suggested that the genetic repertoire of BP9 belongs to open-type genome species. A comparative analysis of a pan-genome dataset using the Kyoto Encyclopedia of Genes and Genomes (KEGG) and Cluster of Orthologous Gene groups (COG) revealed the diversity of secondary metabolic pathways, where BP9 distinguishes itself by exhibiting a greater prevalence of loci associated with the metabolism and transportation of organic and inorganic substances, carbohydrate and amino acid for effective inhabitation in diverse environments. The primary secondary metabolites and their genes involved in synthesizing bacillibactin, fencing, bacitracin, and lantibiotics were identified as acquired through a recent Horizontal gene transfer (HGT) event, which contributes to a significant part of the strain`s antimicrobial potential. Finally, we report some genes essential for plant-host interaction identified in BP9, which reduce spore germination and virulence of multiple fungal and bacterial species. The effective colonization, diverse predicted metabolic pathways and secondary metabolites (antibiotics) suggest testing the suitability of strain BP9 as a potential bio-preparation in agricultural fields.http://www.sciencedirect.com/science/article/pii/S2001037023003550Bacillus paralichenformisEvolutionPan genomeCore genomeSecondary metabolitesPeptides
spellingShingle Muhammad Asif
Zhang Li-Qun
Qingchao Zeng
Muhammad Atiq
Khalil Ahmad
Aqil Tariq
Nadhir Al-Ansari
Jochen Blom
Linda Fenske
Hissah Abdulrahman Alodaini
Ashraf Atef Hatamleh
Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanism
Computational and Structural Biotechnology Journal
Bacillus paralichenformis
Evolution
Pan genome
Core genome
Secondary metabolites
Peptides
title Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanism
title_full Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanism
title_fullStr Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanism
title_full_unstemmed Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanism
title_short Comprehensive genomic analysis of Bacillus paralicheniformis strain BP9, pan-genomic and genetic basis of biocontrol mechanism
title_sort comprehensive genomic analysis of bacillus paralicheniformis strain bp9 pan genomic and genetic basis of biocontrol mechanism
topic Bacillus paralichenformis
Evolution
Pan genome
Core genome
Secondary metabolites
Peptides
url http://www.sciencedirect.com/science/article/pii/S2001037023003550
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