Whole genome analysis of Bacillus amyloliquefaciens TA-1, a promising biocontrol agent against Cercospora arachidicola pathogen of early leaf spot in Arachis hypogaea L.

Publisher: BioMed Central Country of Publication: England NLM ID: 100967807 Publication Model: Electronic Cited Medium: Internet ISSN: 1471-2229 (Electronic) Linking ISSN: 14712229 NLM ISO Abbreviation: BMC Plant Biol Subsets: MEDLINE

Original Publication: London : BioMed Central, [2001-

Bacillus amyloliquefaciens*/genetics ; Fungicides, Industrial*; Arachis/genetics ; Mycosphaerella

Background: Early leaf spot disease, caused by Cercospora arachidicola, is a devastating peanut disease that has severely impacted peanut production and quality. Chemical fungicides pollute the environment; however, Bacillus bacteria can be used as an environmentally friendly alternative to chemical fungicides. To understand the novel bacterial strain and unravel its molecular mechanism, De novo whole-genome sequencing emerges as a rapid and efficient omics approach.
Results: In the current study, we identified an antagonistic strain, Bacillus amyloliquefaciens TA-1. In-vitro assay showed that the TA-1 strain was a strong antagonist against C. arachidicola, with an inhibition zone of 88.9 mm. In a greenhouse assay, results showed that the TA-1 strain had a significant biocontrol effect of 95% on peanut early leaf spot disease. De novo whole-genome sequencing analysis, shows that strain TA-1 has a single circular chromosome with 4172 protein-coding genes and a 45.91% guanine and cytosine (GC) content. Gene function was annotated using non-redundant proteins from the National Center for Biotechnology Information (NCBI), Swiss-Prot, the Kyoto Encyclopedia of Genes and Genomes (KEGG), clusters of orthologous groups of proteins, gene ontology, pathogen-host interactions, and carbohydrate-active enZYmes. antiSMASH analysis predicted that strain TA-1 can produce the secondary metabolites siderophore, tailcyclized peptide, myxochelin, bacillibactin, paenibactin, myxochelin, griseobactin, benarthin, tailcyclized, and samylocyclicin.
Conclusion: The strain TA-1 had a significant biological control effect against peanut early leaf spot disease in-vitro and in greenhouse assays. Whole genome analysis revealed that, TA-1 strain belongs to B. amyloliquefaciens and could produce the antifungal secondary metabolites.
(© 2023. BioMed Central Ltd., part of Springer Nature.)

Al-Raish SM, Saeed EE, Sham A, Alblooshi K, El-Tarabily KA, AbuQamar SF. Molecular characterization and disease control of stem canker on royal poinciana (Delonix regia) caused by Neoscytalidium dimidiatum in the United Arab Emirates. Int J Mole Sci. 2020;21:1033. https://doi.org/10.3390/ijms21031033. (PMID: 10.3390/ijms21031033)
El-Saadony MT, Saad AM, Soliman SM, Salem HM, Ahmed AI, Mahmood M, El-Tahan AM, et al. Plant growthpromoting microorganisms as biocontrol agents of plant diseases: mechanisms, challenges and future perspectives. Front Plant Sci. 2022;13:923880. https://doi.org/10.3389/fpls.2022.923880. (PMID: 10.3389/fpls.2022.923880362755569583655)
Jain A, Sarsaiya S, Wu Q, Lu Y, Shi J. A review of plant leaf fungal diseases and its environment speciation. Bioengin. 2019;10(1):409–24. https://doi.org/10.1080/21655979.2019.1649520. (PMID: 10.1080/21655979.2019.1649520)
Li S, Xue X, Gao M, Wang N, Cui X, Sang S. Genome Resource for Peanut web Blotch Causal Agent Peyronellaea arachidicola strain YY187. Plant Dis. 2021;105(4):1177–8. https://doi.org/10.1094/PDIS-04-20-0898-A. (PMID: 10.1094/PDIS-04-20-0898-A32787658)
Gong L, Han S, Yuan M, Ma X, Hagan A, He G. Transcriptomic analyses reveal the expression and regulation of genes associated with resistance to early leaf spot in peanut. BMC Res Notes. 2020;13(1):381. https://doi.org/10.1186/s13104-020-05225-9. (PMID: 10.1186/s13104-020-05225-9327820197418390)
Braun U, Nakashima C, Crous PW. Cercosporoid fungi (Mycosphaerellaceae) 1Species on other fungi, Pteridophyta and Gymnospermae. IMA Fungus 4. 2013;265–345. https://doi.org/10.5598/imafungus.2013.04.02.12 . 2.
Braun U, Crous PW, Nakashima C. Cercosporoid fungi (Mycosphaerellaceae) species on dicots (Anacardiaceae to Annonaceae). IMA Fungus. 2016;7(1):161–216. https://doi.org/10.5598/imafungus.2016.07.01.10. (PMID: 10.5598/imafungus.2016.07.01.10274334464941684)
Devi PI, Manjula M, Bhavani RV. Agrochemicals, Environment, and Human Health. Annu Rev Environ Resour. 2022;47:399–421. https://doi.org/10.1146/annurev-environ-120920-111015. (PMID: 10.1146/annurev-environ-120920-111015)
Lahlali R, Ezrari S, Radouane N, Kenfaoui J, Esmaeel Q, Hamss E. H. (2022). Biological Control of Plant Pathogens: A Global Perspective. Microorganisms. 10 (3), 596. https://doi.org/10.3390/microorganisms10030596.
He C, He H, Amalin DM, Liu W, Alvindia DG, Zhan J. Biological Control of Plant Diseases: an evolutionary and eco-economic consideration. Pathogens. 2021;10(10). https://doi.org/10.3390/pathogens10101311.
Xu J, Zhang N, Wang K, Xian Q, Dong J, Chen X. Exploring new strategies in diseases resistance of horticultural crops. Front Sustainable Food Syst. 2022;6:1021350. https://doi.org/10.3389/fsufs.2022.1021350. (PMID: 10.3389/fsufs.2022.1021350)
Jaiswal DK, Gawande SJ, Soumia PS, et al. Biocontrol strategies: an eco-smart tool for integrated pest and diseases management. BMC Microbiol. 2022;22:324. https://doi.org/10.1186/s12866-022-02744-2. (PMID: 10.1186/s12866-022-02744-2365818469801620)
Villarreal-Delgado MF, Villa-Rodríguez ED, CiraChávez LA, Estrada-Alvarado MI, Parra-Cota FI, Delos SVS. The genus Bacillus as a biological control agent and its implications in the agricultural biosecurity. Rev Mex Fitopatol. 2017;36(1):95–130. https://doi.org/10.18781/R.MEX.FIT.1706-5. (PMID: 10.18781/R.MEX.FIT.1706-5)
Petrillo C, Castaldi S, Lanzilli M, Selci M, Cordone A, Giovannelli D. Genomic and physiological characterization of Bacilli isolated from salt-pans with Plant Growth promoting features. Front Microbiol. 2021;12:715678. https://doi.org/10.3389/fmicb.2021.715678. (PMID: 10.3389/fmicb.2021.715678345890738475271)
Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H. Bacillus as potential probiotics: status, concerns, and future perspectives. Front Microbiol. 2017;8:1490. https://doi.org/10.3389/fmicb.2017.01490. (PMID: 10.3389/fmicb.2017.01490288485115554123)
Shafi J, Tian H, Ji M. (2017). Bacillus species as versatile weapons for plant pathogens: A review. Biotechnol. Biotechnol. Equip. 2017, 31, 446–45. https://doi.org/10.1080/13102818.2017.1286950.
Chowdhury SP, Hartmann A, Gao XW, Borriss R. Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42-a review. Front Microbiol. 2015;6:780. https://doi.org/10.3389/fmicb.2015.00780. (PMID: 10.3389/fmicb.2015.00780262840574517070)
Saravanakumar D, Thomas A, Banwarie N. Antagonistic potential of lipopeptide producing Bacillus amyloliquefaciens against major vegetable pathogens. Eur J Plant Pathol. 2019;154:319–35. https://doi.org/10.1007/s10658-018-01658-y. (PMID: 10.1007/s10658-018-01658-y)
Ho TH, Chuang CY, Zheng JL, Chen HH, Liang YS, Huang TP, et al. Bacillus amyloliquefaciens strain PMB05 intensififies plant immune responses to confer resistance against bacterial wilt of tomato. Phytopathol. 2020;110:1877–85. (PMID: 10.1094/PHYTO-01-20-0026-R)
Chen J, Liu T, Wei M, Zhu Z, Liu W, Zhang Z. Macrolactin a is the key antibacterial substance of Bacillus amyloliquefaciens D2WM against the pathogen Dickeya chrysanthemi. Eur J Plant Pathol. 2019;155(2):393–404. https://doi.org/10.1007/s10658-019-01774-3. (PMID: 10.1007/s10658-019-01774-3)
Khan M, Salman M, Jan SA, Shinwari ZK. Biological control of fungal phytopathogens: a comprehensive review based on Bacillus species. MOJ Biol Med. 2021;6(2):90–2. https://doi.org/10.15406/mojbm.2021.06.00137. (PMID: 10.15406/mojbm.2021.06.00137)
Zou QX, Ren ZH, Gao SH, Zhou H, Zhao JH, Liu EM. Isolation and identification of Bacillus subtilis YN145 against Magnaporthe oryzae and its antimicrobial activities[J]. Chin J Biol Control. 2017;33(3):421–6.
Fadiji AE, Babalola OO. Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front Bioengin Biotechnol. 2020;8:467. https://doi.org/10.3389/fbioe.2020.00467. (PMID: 10.3389/fbioe.2020.00467)
Gamalero E, Bona E, Glick BR. (2022). Current Techniques to Study Beneficial Plant-Microbe Interactions. Microorganisms 2022, 10, 1380. org/10.3390.
Zeng Q, Xie J, Li Y, Gao T, Xu C, Wang Q. Comparative genomic and functional analyses of four sequenced Bacillus cereus genomes reveal conservation of genes relevant to plant-growth-promoting traits. Sci Rep. 2018;8:17009. https://doi.org/10.1038/s41598-018-35300-y. (PMID: 10.1038/s41598-018-35300-y304519276242881)
Ben Khedher M, Ghedira K, Rolain JM, Ruimy R, Croce O. Application and challenge of 3rd generation sequencing for clinical bacterial studies. Int J Mol Sci. 2022;323:1395. https://doi.org/10.3390/ijms23031395. (PMID: 10.3390/ijms23031395)
Tyler AD, Mataseje L, Urfano CJ, Schmidt L, Antonation KS, Mulvey MR, et al. Evaluation of Oxford Nanopore’s MinION sequencing device for microbial whole genome sequencing applications. Sci Rep. 2018;19(1):10931. https://doi.org/10.1038/s41598-018-29334-5. (PMID: 10.1038/s41598-018-29334-5)
Chavali AK, Rhee SY. Bioinformatics tools for the identification of gene clusters that biosynthesize specialized metabolites. Brief Bioinform. 2018;19(5):1022–34. https://doi.org/10.1093/bib/bbx020. (PMID: 10.1093/bib/bbx02028398567)
Fedorova ND, Moktali V, Medema MH. Bioinformatics approaches and software for detection of secondary metabolic gene clusters. Methods Mol Biol. 2012;944:23–45. https://doi.org/10.1007/978-1-62703-122-6_2. (PMID: 10.1007/978-1-62703-122-6_223065606)
Zhao Y, Wu J, Yang J, Sun S, Xiao J, Yu J. (2012). PGAP: pan-genomes analysis pipeline. Bioinformatics. 1;28(3):416-8. https://doi.org/10.1093/bioinformatics/btr655.
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;W182–5. https://doi.org/10.1093/nar/gkm321 . 35(Web Server issue).
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, Medema MH, Weber T. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res. 2021;49(W1):W29. https://doi.org/10.1093/nar/gkab335. (PMID: 10.1093/nar/gkab335339787558262755)
Anco JD, Thomas SJ, Jordan LD, Shew BB, Monfort SW, Mehl LH, et al. Peanut yield loss in the Presence of Defoliation caused by late or early Leaf Spot. Plant Dis. 2020;104(5):1390–9. https://doi.org/10.1094/PDIS-11-19-2286-RE. (PMID: 10.1094/PDIS-11-19-2286-RE32223639)
Dimopoulou A, Theologidis I, Benaki D, Koukounia M, Zervakou A, Tzima A, Diallinas G et al. (2021). Direct antibiotic activity of Bacillibactin broadens the Biocontrol Range of Bacillus amyloliquefaciens MBI600. mSphere. 6(4):e0037621. https://doi.org/10.1128/mSphere.00376-21.
Tan S, Dong Y, Liao H, Huang J, Song S, Xu, and Y., et al. Antagonistic bacterium Bacillus amyloliquefaciens induces resistance and controls the bacterial wilt of tomato. Pest Manag Sci. 2013;69:1245–52. https://doi.org/10.1002/ps.3491. (PMID: 10.1002/ps.349123519834)
Zalila-Kolsi I, Mahmoud AB, Ali H, Sellami S, Nasfi Z, Tounsi S. Antagonist effects of Bacillus spp. strains against Fusarium graminearum for protection of durum wheat (Triticum turgidum L. subsp. durum). Microbiol Res. 2016;192:148–58. https://doi.org/10.1016/j.micres.2016.06.012. (PMID: 10.1016/j.micres.2016.06.01227664733)
Zhao Y, Selvaraj JN, Xing F, Zhou L, Wang Y, Song H et al. (2014). Antagonistic action of Bacillus subtilis strain SG6 on Fusarium graminearum. PLoS ONE 2014, 9, e92486. https://doi.org/10.1371/journal.pone.0092486.
Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A, Chaumeil PA, et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36:996–1004. https://doi.org/10.1038/nbt.4229. (PMID: 10.1038/nbt.422930148503)
Chen T, Zhang Z, Li W, Chen J, Chen X, Wang B, et al. Biocontrol potential of Bacillus subtilis CTXW 7-6-2 against kiwifruit soft rot pathogens revealed by whole-genome sequencing and biochemical characterisation. Front Microbiol. 2022;13:1069109. https://doi.org/10.3389/fmicb.2022.1069109. (PMID: 10.3389/fmicb.2022.1069109365324989751376)
Chen XH, Koumoutsi A, Scholz R, Schneider K, Vater J, Süssmuth R, et al. Genome analysis of Bacillus amyloliquefaciens FZB42 reveals its potential for biocontrol of plant pathogens. J Biotechnol. 2009;140:27–37. https://doi.org/10.1016/j.jbiotec.2008.10.011. (PMID: 10.1016/j.jbiotec.2008.10.01119041913)
Pinto C, Sousa S, Froufe H, Egas C, Clément C, Fontaine F, Gomes CA. Draft genome sequence of Bacillus amyloliquefaciens subsp. plantarum strain Fito_F321, an endophyte microorganism from Vitis vinifera with biocontrol potential. Stand in Genomic Sci. 2018;13:30. https://doi.org/10.1186/s40793-018-0327-x. (PMID: 10.1186/s40793-018-0327-x)
Zhao Q, Wang L, Luo Y. Recent advances in Natural Products Exploitation in Streptomyces via Synthetic Biology. Eng Life Sci. 2019;19:452–62. https://doi.org/10.1002/elsc.201800137. (PMID: 10.1002/elsc.201800137326250226999378)
Sarmiento-Vizcaíno A, Martín J, Reyes F, García LA, Blanco G. Bioactive Natural Products in Actinobacteria isolated in Rainwater from Storm Clouds transported by western winds in Spain. Front Microbiol. 2021;12:773–095. https://doi.org/10.3389/fmicb.2021.773095. (PMID: 10.3389/fmicb.2021.773095)
Nikoli´ CI, Beri´ CT, Dimki´ CI, Popovi´,C T, Lozo J, Fira D et al. (2019). Biological control of Pseudomonas syringae pv. aptata on sugar beet with Bacillus pumilus SS-10.7 and Bacillus amyloliquefaciens (SS-12.6 and SS-38.4) strains. J. Appl. Microbiol 2019, 126, 165–176. https://doi.org/10.1111/jam.14070.
Du Y, Wang T, Jiang J, Wang Y, Lv C, Sun K, et al. Biological control and plant growth promotion properties of Streptomyces albidoflavus St-220 isolated from Salvia miltiorrhiza rhizosphere. Front Plant Sci. 2022;13:976813. https://doi.org/10.3389/fpls.2022.976813. (PMID: 10.3389/fpls.2022.976813361103649468599)
Roy EM, Griffith KL. Characterization of a novel iron acquisition activity that coordinates the iron response with population density under iron-replete conditions in Bacillus subtilis. J Bacteriol. 2017;199:e00487–16. https://doi.org/10.1128/JB.00487-16. (PMID: 10.1128/JB.00487-1627795321)

LJKMZ20221044 Basic scientific research projects of colleges and universities in Liaoning Province

Keywords: Bacillus amyloliquefaciens; Biocontrol; Cercospora arachidicola; Peanut early leaf spot; Secondary metabolites

0 (Fungicides, Industrial)

Mycosphaerella arachidis

Date Created: 20230904 Date Completed: 20230906 Latest Revision: 20231121

20250114

PMC10478280

10.1186/s12870-023-04423-4

37667202