Biocontrol Potential, Genome and Nonribosomal Peptide Synthetase Gene Expression of Bacillus velezensis 2211
Main Article Content
Abstract
Members of the genus Bacillus produced a diverse group of antimicrobial compounds. Here, we presented the antifungal activity and genome sequence analysis of Bacillus sp. 2211, a potential plant-growth-promoting bacterium. Bacterial supernatants from strain 2211 cultures in nutrient broth (NB) and potato dextrose broth (PDB) suppressed the mycelial growth of Pyricularia oryzae, Colletotrichum aenigma, Colletotrichum fructicola and Fusarium oxysporum. The supernatants were also able to suppress spore germination of these fungi, except for F. oxysporum. However, the supernatant from PDB displayed a significantly higher inhibition activity than NB. Additionally, the supernatant from PDB significantly reduced the disease severity caused by P. oryzae on rice seedlings. The genome of strain 2211 was sequenced. The highest digital DNA-DNA hybridization (80.1%) and average nucleotide identity (97.57%) levels indicated that strain 2211 was a member of the species Bacillus velezensis. The phylogenomic analysis showed that it clustered with B. velezensis NRRL B-41580T, B. velezensis KACC 13105 and B. velezensis subsp. plantarum FZB42T. The gene expression analysis showed the up-regulation of nonribosomal peptide synthetase (NRPS) genes bmyA, fenB and dhbE in PDB, compared to NB. This work demonstrated that the culture media affected the antagonistic activity of strain 2211 possibly through the modification of NRPS biosynthesis genes.
Keywords: Bacillus; antagonistic activity; Pyricularia oryzae; Colletotrichum aenigma; Colletotrichum fructicola
*Corresponding author: Tel.: (+66) 3324-800 Fax: (+66) 324-8424
E-mail: chokchai.ki@kmitl.ac.th
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Copyright Transfer Statement
The copyright of this article is transferred to Current Applied Science and Technology journal with effect if and when the article is accepted for publication. The copyright transfer covers the exclusive right to reproduce and distribute the article, including reprints, translations, photographic reproductions, electronic form (offline, online) or any other reproductions of similar nature.
The author warrants that this contribution is original and that he/she has full power to make this grant. The author signs for and accepts responsibility for releasing this material on behalf of any and all co-authors.
Here is the link for download: Copyright transfer form.pdf
References
Olanrewaju, O.S., Glick, B.R. and Babalola, O.O., 2017. Mechanisms of action of plant growth promoting bacteria. World Journal of Microbiology and Biotechnology, 33(11), DOI: 10.1007/s11274-017-2364-9.
Fira, D., Dimkić, I., Berić, T., Lozo, J. and Stanković, S., 2018. Biological control of plant pathogens by Bacillus species. Journal of Biotechnology, 285, 44-55.
Süssmuth, R.D. and Mainz, A., 2017. Nonribosomal peptide synthesis-principles and prospects. Angew Chemie - International Edition in English, 56, 3770-3821.
Aleti, G., Sessitsch, A. and Brader, G., 2015. Genome mining: Prediction of lipopeptides and polyketides from Bacillus and related Firmicutes. Computational and Structural Biotechnolgy Journal, 13, 192-203.
Tapi, A., Chollet-Imbert, M., Scherens, B. and Jacques P., 2010. New approach for the detection of non-ribosomal peptide synthetase genes in Bacillus strains by polymerase chain reaction. Applied Microbiology and Biotechnology, 85, 1521-1531.
Ngalimat, M.S., Yahaya, R.S.R., Baharudin, M.M.A.A., Yaminudin, S.M., Karim, M., Ahmad, S.A. and Sabri, S., 2021. A review on the biotechnological applications of the operational group Bacillus amyloliquefaciens. Microorganisms, 9, DOI: 10.3390/micro organisms9030614.
Fan, B., Wang, C., Song, X., Ding, X., Wu, L., Wu, H., Gao, X. and Borriss, R., 2018. Bacillus velezensis FZB42 in 2018: The gram-positive model strain for plant growth promotion and biocontrol. Frontiers in Microbiology, 9, DOI: 10.3389/fmicb.2018.02491.
Apimeteethamrong, S. and Kittiwongwattana, C., 2019 Diversity and plant growth promoting activities of rice epiphytic bacteria. Current Applied Science and Technology, 19, 66-79.
Apimeteethamrong, S. and Kittiwongwattana, C., 2021 Medium effect on antagonistic activity and detection of nonribosomal peptide synthetase genes in epiphytic Bacillus strains. Current Applied Science and Technology, 4, 637-651.
Sun, P., Cui, J., Jia, X. and Wang, W., 2017. Isolation and characterization of Bacillus amyloliquefaciens L-1 for biocontrol of pear ring rot. Horticultural Plant Journal, 3, 183-189.
Nuwong, W. and Kittiwongwattana, C., 2022. Correlation of antifungal activities and nonribosomal peptide synthetase gene expression of Bacillus siamensis 1021. Chiang Mai Journal of Science, 49, 272-283.
International Rice Research Institute, 2002. Standard Evaluation System for Rice. Manila: International Rice Research Institute.
Awla, H.K., Kadir, J., Othman, R., Rashid, T.S., Hamid, S. and Wong, M.Y., 2017. Plant growth-promoting abilities and biocontrol efficacy of Streptomyces sp. UPMRS4 against Pyricularia oryzae. Biological Control, 112, 55-63.
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., Pyshkin, A.V., Sirotkin, A.V., Vyahhi, N., Tesler, G., Alekseyev, M.A. and Pevzner, P.A., 2012. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19, 455-477.
Richter, M., Rosselló-Móra, R., Oliver, G.F. and Peplies, J., 2016. JSpeciesWS: A web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics, 32, 929-931.
Meier-Kolthoff, J.P. and Göker, M., 2019. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nature Communications, 10, DOI: 10.1038/ s41467-019-10210-3.
Tatusova, T., Dicuccio, M., Badretdin, A., Chetvernin, V., Nawrocki, E.P., Zaslavsky, L., Lomsadze, A., Pruitt, K.D., Borodovsky, M. and Ostell, J., 2016. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Research, 19, 6614-6624.
Darling, A.E., Mau, B. and Perna, N.T., 2010. progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLoS One, 25, DOI: 10.1371/journal. pone.0011147.
Dieckmann, M.A., Beyvers, S., Nkouamedjo-Fankep, R.C., Hanel, P.H.G., Jelonek, L., Blom, J. and Goesmann, A., 2021. EDGAR3.0: Comparative genomics and phylogenomics on a scalable infrastructure. Nucleic Acids Research, 49, W185-W192.
Blin, K., Shaw, S., Kloosterman, A.M., Charlop-Powers, Z., van Wezel, G.P., Medema, M.H. and Weber, T., 2021. AntiSMASH 6.0: Improving cluster detection and comparison capabilities. Nucleic Acids Research, 49, W29-W35.
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M. and Rozen, S.G., 2012. Primer3-new capabilities and interfaces. Nucleic Acids Research, 40, DOI: 10.1093/nar/gks596.
Livak, K.J. and Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25, 402-408.
Sun, D., Liao, J., Sun, L., Wang, Y., Liu, Y., Deng, Q., Zhang, N., Xu, D., Fang, Z., Wang, W. and Gooneratne, R., 2019. Effect of media and fermentation conditions on surfactin and iturin homologues produced by Bacillus natto NT-6: LC–MS analysis. AMB Express, 9, DOI: 10.1186/s13568-019-0845-y.
Xu, W., Ren, H., Ou, T., Lei, T., Wei, J., Huang, C., Li, T., Strobel, G., Zhou, Z. and Xie, J., 2019. Genomic and functional characterization of the endophytic Bacillus subtilis 7PJ-16 strain, a potential biocontrol agent of mulberry fruit sclerotiniose. Microbial Ecology, 77, 651-663.
Tian, Z., Chen, C., Chen, K., Liu, P., Fan, Q., Zhao, J. and Long, C., 2020. Biocontrol and the mechanisms of Bacillus sp. w176 against postharvest green mold in citrus. Postharvest Biology and Technology, 159, DOI: 10.1016/j.postharvbio.2019.111022.
Alijani, Z., Amini, J., Ashengroph, M., Bahramnejad, B. and Mozafari, A.A., 2021. Biocontrol of strawberry anthracnose disease caused by Colletotrichum nymphaeae using Bacillus atrophaeus strain DM6120 with multiple mechanisms. Tropical Plant Pathology, 47, 245-259.
Lu, H., Qian, S., Muhammad, U., Jiang, X., Han, J. and Lu, Z., 2016. Effect of fructose on promoting fengycin biosynthesis in Bacillus amyloliquefaciens fmb-60. Journal of Applied Microbiology, 121, 1653-1664.
Rong, S., Xu, H., Li, L., Chen, R., Gao, X. and Xu, Z., 2020. Antifungal activity of endophytic Bacillus safensis B21 and its potential application as a biopesticide to control rice blast. Pesticide Biochemistry and Physiology, 162, 68-77.
Zhang, L. and Sun, C., 2018. Fengycins, cyclic lipopeptides from marine Bacillus subtilis strains, kill the plant-pathogenic fungus Magnaporthe grisea by inducing reactive oxygen species production and chromatin condensation. Applied and Environmental Microbiology, 84(18), DOI: 10.1128/AEM.00445-18.
Chun, J., Oren, A., Ventosa, A., Christensen, H., Arahal, D.R., da Costa, M.S., Rooney, A.P., Yi, H., Xu, X., Meyer, S.D. and Trujillo, M.E., 2018. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 68, 461-466.
Fan, B., Blom, J., Klenk, H.P. and Borriss, R., 2017. Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis form an “Operational Group B. amyloliquefaciens” within the B. subtilis species complex. Frontiers in Microbiology, 8, 22, DOI: 10.3389/fmicb.2017.00022.
Ruiz-García, C., Béjar, V., Martínez-Checa, F., Llamas, I. and Quesada, E., 2005. Bacillus velezensis sp. nov., a surfactant-producing bacterium isolated from the river Vélez in Málaga, southern Spain. International Journal of Systematic and Evolutionary Microbiology, 55, 191-195.
Wang, L.T., Lee, F.L., Tai, C.J. and Kuo, H.P., 2008. Bacillus velezensis is a later heterotypic synonym of Bacillus amyloliquefaciens. International Journal of Systematic and Evolutionary Microbiology, 58, 671-675.
Dunlap, C.A., Kim, S.J., Kwon, S.W. and Rooney, A.P., 2016. Bacillus velezensis is not a later heterotypic synonym of Bacillus amyloliquefaciens; Bacillus methylotrophicus, Bacillus amyloliquefaciens subsp. plantarum and ‘Bacillus oryzicola’ are later heterotypic synonyms of Bacillus velezensis based on phylogenomics. International Journal of Systematic and Evolutionary Microbiology, 66, 1212-1217.
Cai, X.C., Liu, C.H., Wang, B.T. and Xue, Y.R., 2017. Genomic and metabolic traits endow Bacillus velezensis CC09 with a potential biocontrol agent in control of wheat powdery mildew disease. Microbiological Reseach, 196, 89-94.
Chen, L., Heng, J., Qin, S. and Bian, K., 2018. A comprehensive understanding of the biocontrol potential of Bacillus velezensis LM2303 against Fusarium head blight. PLoS One, 13(6), DOI: 10.1371/journal.pone.0198560.
Jiang, C.H., Liao, M.J., Wang, H.K., Zheng, M.Z., Xu, J.J. and Guo, J.H., 2018. Bacillus velezensis, a potential and efficient biocontrol agent in control of pepper gray mold caused by Botrytis cinerea. Biological Control, 126, 147-57.
Chen, Z., Zhao, L., Chen, W., Dong, Y., Yang, C., Li, C., Hong, X., Gao, X., Chen, R., Li, L. and Xu, Z., 2020. Isolation and evaluation of Bacillus velezensis ZW-10 as a potential biological control agent against Magnaporthe oryzae. Biotechnology and Biotechnological Equipment, 34, 714-724.
Prasanna, S., Prasannakumar, M.K., Mahesh, H.B., Babu, G.V., Kirnaymayee, P., Puneeth, M.E., Narayan, K.S. and Pramesh, D., 2021. Diversity and biopotential of Bacillus velezensis strains A6 and P42 against rice blast and bacterial blight of pomegranate. Archives of Microbiology, 203, 4189-4199.
Chen, Z., Zhao, L., Dong, Y., Chen, W., Li, C., Gao, X., Chen, R., Li, L. and Xu, Z., 2021. The antagonistic mechanism of Bacillus velezensis ZW10 against rice blast disease: Evaluation of ZW10 as a potential biopesticide. PLoS One, 16(8), DOI: 10.1371/journal. pone.0256807.
Steinke, K., Mohite, O.S,, Weber, T. and Kovács, Á.T., 2021. Phylogenetic distribution of secondary metabolites in the Bacillus subtilis species complex. mSystems, 6(2), DOI: 10.1128/mSystems.00057-21.
Salazar, B., Ortiz, A., Keswani, C., Minkina, T., Mandzhieva, S., Singh S.P., Rekadwad, B., Borriss, R., Jain, A., Singh, H.B. and Sansinenea, E., 2022. Bacillus spp. as bio-factories for antifungal secondary metabolites: Innovation beyond whole organism formulations. Microbial Ecology, DOI: 10.1007/s00248-022-02044-2.
Lam, V.B., Meyer, T., Arias, A.A., Ongena, M., Oni, F.E. and Höfte, M., 2021. Bacillus cyclic lipopeptides iturin and fengycin control rice blast caused by Pyricularia oryzae in potting and acid sulfate soils by direct antagonism and induced systemic resistance. Microorganisms, 9, DOI: 10.3390/microorganisms9071441.
Liao, J.H., Chen, P.Y., Yang, Y.L., Kan, S.C., Hsieh, F.C. and Liu, Y.C., 2016. Clarification of the antagonistic effect of the lipopeptides produced by Bacillus amyloliquefaciens BPD1 against Pyricularia oryzae via in situ MALDI-TOF IMS analysis. Molecules, 21, DOI: 10.3390/molecules21121670.
Amruta, N., Prasanna Kumar, M.K., Puneeth, M.E., Sarika, G., Kandikattu, H.K., Vishwanath, K. and Narayanaswamym, S., 2018. Exploring the potentiality of novel rhizospheric bacterial strains against the rice blast fungus Magnaporthe oryzae. Plant Pathology Journal, 34, 126-138.
Deleu, M., Paquot, M. and Nylander, T., 2008. Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. Biophysical Journal, 94, 2667-2779.
Nithyapriya, S., Lalitha, S., Sayyed, R.Z., Reddy, M.S., Dailin, D.J., Enshasy, H.A.E., Surianni, N.L. and Herlambang, S., 2021. Production, purification, and characterization of bacillibactin siderophore of bacillus subtilis and its application for improvement in plant growth and oil content in sesame. Sustainability, 13, DOI: 10.3390/su13105394.
Sun, J., Liu, Y., Lin, F., Lu, Z. and Lu, Y., 2021. CodY, ComA, DegU and Spo0A controlling lipopeptides biosynthesis in Bacillus amyloliquefaciens fmbJ. Journal of Applied Microbiology, 131, 1289-1304.
Wang, P., Guo, Q., Ma, Y., Li, S., Lu, X., Zhang, X. and Ma, P., 2015. DegQ regulates the production of fengycin and biofilm formation of the biocontrol agent Bacillus subtilis NCD-2. Microbiological Research, 178, 42-50.
Xu, Z., Xie, J., Zhang, H., Wang, D., Shen, Q. and Zhang, R., 2018. Enhanced control of plant wilt disease by a xylose-inducible degQ gene engineered into Bacillus velezensis strain SQR9XYQ. Biological Control, 109, 36-43.