A new <em>Peribacillus simplex</em> d27.3 strain mediates antimicrobial activity through a combination of secondary metabolites, including fengycins

Margarita Baranova; Maria Romanenko; Iuliia Savina; Ekaterina Pilipenko; Olga Belozerova; Stanislav Terekhov; Anton Nizhnikov; Kirill Antonets; Ivan Smirnov

doi:10.21638/spbu03.2024.206

Authors

Margarita Baranova Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, ul. Miklukho-Maklaya, 16/10, Moscow, 117997, Russian Federation https://orcid.org/0000-0002-1759-9836
Maria Romanenko Laboratory for Proteomics of Supra-Organismal Systems, All-Russia Research Institute for Agricultural Microbiology, chosse Podbel'skogo, 3, Saint Petersburg, 196608, Russian Federation; Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-3990-4336
Iuliia Savina Laboratory for Proteomics of Supra-Organismal Systems, All-Russia Research Institute for Agricultural Microbiology, chosse Podbel'skogo, 3, Saint Petersburg, 196608, Russian Federation https://orcid.org/0009-0005-5104-8543
Ekaterina Pilipenko Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, ul. Miklukho-Maklaya, 16/10, Moscow, 117997, Russian Federation https://orcid.org/0009-0007-4288-3410
Olga Belozerova Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, ul. Miklukho-Maklaya, 16/10, Moscow, 117997, Russian Federation https://orcid.org/0000-0002-5603-5371
Stanislav Terekhov Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, ul. Miklukho-Maklaya, 16/10, Moscow, 117997, Russian Federation https://orcid.org/0000-0003-2220-0452
Anton Nizhnikov Laboratory for Proteomics of Supra-Organismal Systems, All-Russia Research Institute for Agricultural Microbiology, chosse Podbel'skogo, 3, Saint Petersburg, 196608, Russian Federation; Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-8338-3494
Kirill Antonets Laboratory for Proteomics of Supra-Organismal Systems, All-Russia Research Institute for Agricultural Microbiology, chosse Podbel'skogo, 3, Saint Petersburg, 196608, Russian Federation; Department of Genetics and Biotechnology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation https://orcid.org/0000-0002-8575-2601
Ivan Smirnov Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, ul. Miklukho-Maklaya, 16/10, Moscow, 117997, Russian Federation; Department of Chemistry, Lomonosov Moscow State University, Leninskiye Gory, 1-3, Moscow, 119991, Russian Federation https://orcid.org/0000-0002-0384-6568

DOI:

https://doi.org/10.21638/spbu03.2024.206

Abstract

Soil is a classical source of beneficial microorganisms. Soil microbiomes provided the overwhelming majority of antibiotic-producing strains, biocontrol agents, probiotics, and plant-protecting bacteria. The functionality of strains isolated from various soil samples is predetermined by the biosynthetic potential encoded in their genomes. Here, we describe a novel Peribacillus simplex d27.3 strain isolated from the soil sample of a pine forest in the Republic of Dagestan, Russia. P. simplex d27.3 displayed antibiotic activity against gram-positive bacteria and fungi while being inactive against the model hypersensitive gram-negative strain E. coli ΔlptD. Metabolomic analysis revealed that antimicrobial activity was partially mediated by the fengycin lipopetides (C-16 fengycin A, C-17 fengycin A, and C-16 fengycin B). In addition, the P. simplex d27.3 strain was found to produce other hydrophilic and more hydrophobic antimicrobials yet to be described. Thus, the P. simplex d27.3 strain is a producer of useful antimicrobial compounds with a high potential for application in biotechnology and agriculture.

Keywords:

Peribacillus simplex, fengycins, antibiotics, soil microbiome

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References

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. Journal of Molecular Biology 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

Baranova, M. N., Kudzhaev, A. M., Mokrushina, Y. A., Babenko, V. V., Kornienko, M. A., Malakhova, M. V., Yudin, V. G., Rubtsova, M. P., Zalevsky, A., Belozerova, O. A., Kovalchuk, S., Zhuravlev, Y. N., Ilina, E. N., Gabibov, A. G., Smirnov, I. V., and Terekhov, S. S. 2022. Deep functional profiling of wild animal microbiomes reveals probiotic Bacillus pumilus strains with a common biosynthetic fingerprint. International Journal of Molecular Sciences 23(3):1168. https://doi.org/10.3390/ijms23031168

Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C., and Mahillon, J. 2019. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Frontiers in Microbiology 10:302. https://doi.org/10.3389/fmicb.2019.00302

Cochrane, S. A. and Vederas, J. C. 2016. Lipopeptides from Bacillus and Paenibacillus spp.: a gold mine of antibiotic candidates. Medicinal Research Reviews 36(1):4–31. https://doi.org/10.1002/med.21321

Deleu, M., Paquot, M., and Nylander, T. 2005. Fengycin interaction with lipid monolayers at the air-aqueous interface-implications for the effect of fengycin on biological membranes. Journal of Colloid and Interface Science 283(2):358–365. https://doi.org/10.1016/j.jcis.2004.09.036

Deleu, M., Paquot, M., and Nylander, T. 2008. Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. Biophysical Journal 94(7):2667–2679. https://doi.org/10.1529/biophysj.107.114090

Hashem, A., Tabassum, B., and Fathi Abd Allah, E. 2019. Bacillus subtilis: a plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi Journal of Biological Sciences 26(6):1291–1297. https://doi.org/10.1016/j.sjbs.2019.05.004

Kiesewalter, H. T., Lozano-Andrade, C. N., Strube, M. L., and Kovacs, A. T. 2020. Secondary metabolites of Bacillus subtilis impact the assembly of soil-derived semisynthetic bacterial communities. Beilstein Journal of Organic Chemistry 16:2983–2998. https://doi.org/10.3762/bjoc.16.248

Lopes, R., Tsui, S., Goncalves, P. J. R. O., and de Queiroz, M. V. 2018. A look into a multifunctional toolbox: endophytic Bacillus species provide broad and underexploited benefits for plants. World Journal of Microbiology and Biotechnology 34(7):94. https://doi.org/10.1007/s11274-018-2479-7

Luise, D., Bosi, P., Raff, L., Amatucci, L., Virdis, S., and Trevisi, P. 2022. Bacillus spp. probiotic strains as a potential tool for limiting the use of antibiotics, and improving the growth and health of pigs and chickens. Frontiers in Microbiology 13:801827. https://doi.org/10.3389/fmicb.2022.801827

Manetsberger, J., Caballero Gomez, N., Soria-Rodríguez, C., Benomar, N., and Abriouel, H. 2023. Simply versatile: the use of Peribacillus simplex in sustainable agriculture. Microorganisms 11(10):2540. https://doi.org/10.3390/microorganisms11102540

Medeot, D. B., Fernandez, M., Morales, G. M., and Jofre, E. 2020. Fengycins from Bacillus amyloliquefaciens MEP218 exhibit antibacterial activity by producing alterations on the cell surface of the pathogens Xanthomonas axonopodis pv. vesicatoria and Pseudomonas aeruginosa PA01. Frontiers in Microbiology 10:3107. https://doi.org/10.3389/fmicb.2019.03107

Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J., and Setlow, P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiology and Molecular Biology Reviews 64(3):548–572. https://doi.org/10.1128/MMBR.64.3.548-572.2000

Piewngam, P., Zheng, Y., Nguyen, T. H., Dickey, S. W., Joo, H. S., Villaruz, A. E., Glose, K. A., Fisher, E. L., Hunt, R. L., Li, B., Chiou, J., Pharkjaksu, S., Khongthong, S., Cheung, G. Y. C., Kiratisin, P., and Otto, M. 2018. Pathogen elimination by probiotic Bacillus via signalling interference. Nature 562(7728):532–537. https://doi.org/10.1038/s41586-018-0616-y

Punina, N. V., Zotov, V. S., Parkhomenko, A. L., Parkhomenko, T. U., and Topunov, A. F. 2013. Genetic diversity of Bacillus thuringiensis from different geo-ecological regions of Ukraine by analyzing the 16S rRNA and gyrB genes and by AP-PCR and saAFLP. Acta Naturae 5(1):90–100. https://doi.org/10.32607/20758251-2013-5-1-90-100

Rampersad, J., Khan, A., and Ammons, D. 2002. Usefulness of staining parasporal bodies when screening for Bacillus thuringiensis. Journal of Invertebrate Pathology 79(3):203–204. https://doi.org/10.1016/S0022-2011(02)00018-6

Saxena, A. K., Kumar, M., Chakdar, H., Anuroopa, N., and Bagyaraj, D. J. 2020. Bacillus species in soil as a natural resource for plant health and nutrition. Journal of Applied Microbiology 128(6):1583–1594. https://doi.org/10.1111/jam.14506

Sperandeo, P., Lau, F. K., Carpentieri, A., De Castro, C., Molinaro, A., Deho, G., Silhavy, T. J., and Polissi, A. 2008. Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. Journal of Bacteriology 190(13):4460–4469. https://doi.org/10.1128/JB.00270–08

Sumi, C. D., Yang, B. W., Yeo, I. C., and Hahm, Y. T. 2015. Antimicrobial peptides of the genus Bacillus: a new era for antibiotics. Canadian Journal of Microbiology 61(2):93–103. https://doi.org/10.1139/cjm-2014-0613

Tenssay, Z. W., Ashenafi, M., Eiler, A., and Bertilson, S. 2009. Isolation and characterization of Bacillus thuringiensis from soils in contrasting agroecological zones of Ethiopia. SINET: Ethiopian Journal of Science 32(2):117–128. https://doi.org/10.4314/sinet.v32i2.68863

Travers, R. S., Martin, P. A. W., and Reichelderfer, C. F. 1987. Selective process for efficient isolation of soil Bacillus spp. Applied and Environmental Microbiology 53(6):1263–1266. https://doi.org/10.1128/aem.53.6.1263-1266.1987

Vanittanakom, N., Loeffler, W., Koch, U., and Jung, G. 1986. Fengycin — a novel antifungal lipopeptide antibiotic produced by Bacillus subtilis F-29–3. Journal of Antibiotics (Tokyo) 39(7):888–901. https://doi.org/10.7164/antibiotics.39.888

Yin, H., Guo, C., Wang, Y., Liu, D., Lv, Y., Lv, F., and Lu, Z. 2013. Fengycin inhibits the growth of the human lung cancer cell line 95D through reactive oxygen species production and mitochondria-dependent apoptosis. Anticancer Drugs 24(6):5875–98. https://doi.org/10.1097/CAD.0b013e3283611395

Yoo, K., Han, I., Ko, K. S., Lee, T. K., Yoo, H., Khan, M. I., Tiedje, J. M., and Park, J. 2019. Bacillus-dominant airborne bacterial communities identified during Asian dust events. Microbial Ecology 78(3):677–687. https://doi.org/10.1007/s00248-019-01348-0