Genome Insights into the Plant Growth Promoting Features of a Newly Found Microbispora sp. SCL1-1

Main Article Content

Wipawee Dejtisakdi
Thitikorn Duangupama
Chitti Thawai

Abstract

Plant growth-promoting (PGP) actinobacteria can be used to promote plant growth. Their use is a promising strategy that can be employed instead of agricultural chemical fertilizers. An actinobacterium strain, designated SCL1-1, was collected and isolated from a soil sample in a herbal garden at Pathum Thani province, Thailand. Analysis revealed that the SCL1-1 strain was a Gram-positive bacterium that formed longitudinal paired spores that were borne directly on aerial mycelia. It contained meso-diaminopimelic acid in its cell wall peptidoglycan. Moreover, madurose, which is a diagnostic sugar, was present in its whole-cell hydrolysates. 16S rRNA gene analysis revealed that the SCL1-1 strain was a member of the Microbispora and showed a close relationship to Microbispora rosea ATCC 12950T (99.6%), followed by Microbispora hainanensis DSM 45428T (99.2%). However, a genome-based polyphasic study revealed that strain SCL1-1 had a low average nucleotide identity (ANI) (<95%), and digital DNA–DNA hybridization (dDDH) value (<70%) with M. rosea ATCC 12950T and M. hainanensis DSM 45428T, indicating that strain SCL1-1 was a different species to its close relatives. Genome mining of strain SCL1-1 showed the presence of genes related to the production of indole-3-acetic acid (IAA), and siderophore, which are agents that promote plant growth. In addition, the genome of strain SCL1-1 was found in several secondary metabolite biosynthetic gene clusters, which were possibly encoded for a broad range of remarkable natural products and antibiotics.

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References

Bérdy, J., 2005. Bioactive microbial metabolites. The Journal of Antibiotic, 58(1), 1-26, doi:10.1038/ja.2005.1.

Supong, K., Thawai, C., Supothina, S., Auncharoen, P. and Pittayakhajonwut, P., 2016. Antimicrobial and antioxidant activities of quinoline alkaloids from Pseudomonas aeruginosa BCC76810. Phytochemistry Letter, 17, 100-106, https://doi.org/10.1016/j.phytol.2016.07.007.

Silva, G.D.C., Kitano, I.T., Ribeiro, I.A.D.F. and Lacava, P.T., 2022. The potential use of actinomycetes as microbial inoculants and biopesticides in agriculture. Frontiers in Soil Science, 2, https://doi.org/10.3389/fsoil.2022.833181.

Franco, C.M.M., 2012. Genus Microbispora. In: M. Goodfellow, P. Kämpfer, H.-J. Busse, M. E. Trujillo, K.-I. Suzuki, W. Ludwig and W. B. Whitman, eds. Bergey’s Manual of Systematic Bacteriology. Vol 5, The Actinobacteria. New York: Springer, pp. 1831-1838.

Nakajima, Y., Kitpreechavanich, V., Suzuki, K. and Kudo, T., 1999. Microbispora corallina sp. nov., a new species of the genus Microbispora isolated from Thai soil. International Journal of Systematic Bacteriology, 49(4), 1761-1767.

Xu, X.-X., Wang, H.-L., Lin, H.-P., Wang, C., Qu, Z., Xie, Q.-Y., Ruan, J.-S. and Hong, K., 2012. Microbispora hainanensis sp. nov., isolated from rhizosphere soil of Excoecaria agallocha in a mangrove. International Journal of systematic and Evolutionary Microbiology, 62(10), 2430-2434, https://doi.org/10.1099/ijs.0.037267-0.

Miyadoh, S., Amano, S., Tohyama, H. and Shomura, T., 1990. A taxonomic review of the genus Microbispora and a proposal to transfer two species to the genus Actinomadura and to combine ten species into Microbispora rosea. Journal of General Microbiology, 136(9), 1905-1913, https://doi.org/10.1099/00221287-136-9-1905.

Boondaeng, A., Ishida, Y., Tamura, T., Tokuyama, S. and Kitpreechavanich, V., 2009. Microbispora siamensis sp. nov., a thermotolerant actinomycete isolated from soil. International Journal of Systematic Evolutionary Microbiology, 59(12), 3136-3139, https://doi.org/10.1099/ijs.0.009613-0.

Guo, L., Li, Z., Xu, X., Pang, Q. and Zhao, J., 2019. Microbispora sitophila sp. nov., a novel actinobacterium isolated from rhizosphere soil of wheat (Triticum aestivum L.). International Journal of Systematic Evolutionary Microbiology, 71(3), https://doi.org/10.1099/ijsem.0.004684.

Kittisrisopit, S., Pittayakhajonwut, P., Tadtong, S. and Thawai, C., 2018. Microbispora soli sp. nov., isolated from soil of a hot spring. International Journal of Systematic Evolutionary Microbiology, 68(12), 3863-3868, https://doi.org/10.1099/ijsem.0.003075.

Gong, X., Xiang, W., Cao, X., Yu, Y., Hao, Y., Li, L., Wang, Q., Zou, H. and Qian, C., 2020. Microbispora cellulosiformans sp. nov., a novel actinomycete with cellulase activity isolated from soil in the cold region. Antonie Van Leeuwenhoek, 113(12), 2053-2062, https://doi.org/10.1007/s10482-020-01477-4.

Thawai, C., Bunbamrung, N., Pittayakhajonwut, P., Chongruchiroj, S., Pratuangdejkul, J., He, YW., Tadtong, S., Sareedenchai, V., Prombutara, P. and Qian, Y., 2020. A novel diterpene agent isolated from Microbispora hainanensis strain CSR-4 and its in vitro and in silico inhibition effects on acetylcholine esterase enzyme. Scientific Reports, 10(1), 1-18, https://doi.org/10.1038/s41598-020-68009-y.

Okujo, N., Iinuma, H., George, A., Eim, K.S., Li, TL., Ting, N.S., Jye, T.C., Hotta, K., Hatsu, M., Fukagawa, Y., Shibahara, S., Numata, K. and Konda, S., 2007. Bispolides, novel 20-membered ring macrodiolide antibiotics from Microbispora. The Journal of Antibiotic, 60, 216-219, https://doi.org/10.1038/ja.2007.26.

Ivanova, V., Kolarova, M., Aleksieva, K., Gräfe, U., Dahse, H.-M. and Laatsch., H., 2007. Microbiaeratin, a new natural indole alkaloid from a Microbispora aerata strain, isolated from Livingston Island, Antarctica. Preparative Biochemistry and Biotechnology, 37(2), 161-168, https://doi.org/10.1080/10826060701199122.

Nimaichand, S., Devi, A.M. and Li, W.-J., 2016. Direct plant growth-promoting ability of actinobacteria in grain legumes. In: G. Subramaniam, S. Arumugam and V. Rajendran, eds. Plant Growth Promoting Actinobacteria. Singapore: Springer, pp. 1-16.

Ouyang, J., Shao, X. and Li, J., 2000. Indole-3-glycerol phosphate, a branchpoint of indole-3-acetic acid biosynthesis from the tryptophan biosynthetic pathway in Arabidopsis thaliana. Plant Journal, 24(3), 327-333, https://doi.org/10.1046/j.1365-313x.2000.00883.x.

Lambrecht, J.A. and Downs, D.M., 2013. Anthranilate phosphoribosyl transferase (TrpD) generates phosphoribosylamine for thiamine synthesis from enamines and phosphoribosyl pyrophosphate. ACS Chemical Biology, 8(1), 242-248, https://doi.org/10.1021/cb300364k.

Carro, L. and Nouioui, I., 2017. Taxonomy and systematics of plant probiotic bacteria in the genomic era. AIMS Microbiology, 3(3), 383-412, https://doi.org/10.3934/microbiol.2017.3.383.

Müller, W.E.G., Schröder, H.C. and Wang, X., 2019. Inorganic polyphosphates as storage for and generator of metabolic energy in the extracellular matrix. Chemical Reviews, 119(24), 12337-12374, https://doi.org/10.1021/acs.chemrev.9b00460.

Willsky, G.R. and Malamy, M.H., 1980. Characterization of two genetically separable inorganic phosphate transport systems in Escherichia coli. Journal of Bacteriology, 144(1), 356-365, https://doi.org/10.1128/jb.144.1.356-365.1980.

Thawai, C., Rungjindamai, N., Klanbut, K. and Tanasupawat, S., 2017. Nocardia xestospongiae sp. nov., isolated from a marine sponge in the Andaman Sea. International Journal of Systematic and Evolutionary Microbiology, 67(5), 1451-1456, https://doi.org/10.1099/ijsem.0.001736.

Shirling, E.B., and Gottlieb, D., 1966. Methods for characterization of Streptomyces species. International Journal of Systematic and Evolutionary Microbiology, 16, 313-340, http://dx.doi.org/10.1099/00207713-16-3-313.

Thawai, C., Tanasupawat, S., Suwanborirux, K. and Kudo, T., 2010. Actinaurispora siamensis gen. nov., a new member of the family Micromonosporaceae. International Journal of Systematic and Evolutionary Microbiology, 60(7), 1660-1666, http://dx.doi.org/10.1099/ijs.0.013763-0.

Itoh, T., Kudo, T., Parenti, F. and Seino, A., 1989. Amended description of the genus Kineosporia, based on chemotaxonomic and morphological studies. International Journal of Systematic Bacteriology, 39(2), 168-173, http://dx.doi.org/10.1601/nm.7655.

Kelly, K.L., Judd, D.W., Inter-Society Color Council and United States National Bureau of Standards, 1964. ISCC- NBS Color-name Charts Illustrated with Centroid Colors: (Supplement to NBS Circular 553). Washington D.C.: Smithsonian Libraries.

Arai, T., 1975. Culture Media for Actinomycetes. Tokyo: The Society for Actinomycetes.

Williams, S.T. and Cross, T., 1971. Methods in Microbiology: Chapter XI Actinomycetes. Methods in Microbiology, 4, 295-334, https://doi.org/10.1016/S0580-9517(09)70016-9.

Gordon, R.E., Barnett, D.A., Handerhan, J.E., and Pang, C.H.-N., 1974. Nocardia coeliaca, Nocardia autotrophica, and the Nocardin strain. International Journal of Systematic Bacteriology, 24(1), 54-63.

Supong, K., Suriyachadkun, C., Pittayakhajonwut, P., Suwanborirux, K. and Thawai, C., 2013. Micromonospora spongicola sp. nov., an actinomycete isolated from a marine sponge in the Gulf of Thailand. The Journal of antibiotics, 66, 505-509, https://doi.org/10.1038/ja.2013.35.

Phongsopitanun, W., Thawai, C., Suwanborirux, K., Kudo, T., Ohkuma, M. and Tanasupawat, S., 2014. Streptomyces chumphonensis sp. nov., isolated from marine sediments. International Journal of Systematic and Evolutionary Microbiology, 64(8), 2605-2610, https://doi.org/10.1099/ijs.0.062992-0.

Komagata, K. and Suzuki, K.-I., 1988. Lipid and cell-wall analysis in bacterial systematics. Methods Microbiology, 19, 161-207, https://doi.org/10.1016/S0580-9517(08)70410-0.

Uchida, K. and Aida, K., 1984. An improved method for the glycolate test for simple identification of the acyl type of bacterial cell walls. The Journal of General and Applied Microbiology, 30(2), 131-134, https://doi.org/10.2323/jgam.30.131.

Collins, M.D., Pirouz, T., Goodfellow, M. and Minnikin, D.E., 1977. Distribution of menaquinones in actinomycetes and corynebacteria. Journal of General Microbiology, 100(2), 221-230, https://doi.org/10.1099/00221287-100-2-221.

Sasser, M., 1990. Identification of bacteria by gas chromatography of cellular fatty acids. MIDI Technical Note 101, Newark: MIDI.

Kämpfer, P. and Kroppenstedt, RM., 1996. Numerical analysis of fatty acid patterns of icoryneform bacteria and related taxa. Canadian Journal of Microbiology, 42, 989-1005, https://doi.org/10.1139/m96-128.

Kittiwongwattana, C., Thanaboripat, D., Laosinwattana, C., Koohakan, P., Parinthawong N. and Thawai, C., 2015. Micromonospora oryzae sp. nov., isolated from roots of upland rice. International Journal of Systematic and Evolutionary Microbiology, 65, 3818-3823, https://doi.org/10.1099/ijsem.0.000500.

Yoon, S.-H., Ha, S.-M., Kwon, S., Lim, J., Kim, Y., Seo, H. and Chun, J., 2017. Introducing EzBioCloud: A taxonomically united database of 16S rRNA and whole-genome assemblies. International Journal of Systematic and Evolutionary Microbiology, 67(5), 1613-1617, https://doi.org/10.1099/ijsem.0.001755.

Saitou, N. and Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406-425, https://doi.org/10.1093/

oxfordjournals.molbev.a040454.

Felsenstein, J., 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17, 368-376, https://doi.org/10.1007/BF01734359.

Fitch, W.M., 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Biology, 20(4), 406-416, https://doi.org/10.1093/sysbio/20.4.406.

Kumar, S., Stecher, G., Li, M., Knyaz, C. and Tamura, K., 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547-1549, https://doi.org/10.1093/molbev/msy096.

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(5), 455-477, https://doi.org/10.1089/cmb.2012.0021.

Richter, M. and Rosselló-Móra, R., 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proceedings of the National Academy of Sciences of the United States of America, 106(45), 19126-19131, https://doi.org/10.1073/pnas.0906412106.

Richter, M., Rosselló-Móra, R., Glöckner, F.O. and Peplies, J., 2016. J Species WS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics, 32(6), 929-931, https://doi.org/10.1093/bioinformatics/btv681.

Rodriguez-R, L.M. and Konstantinidis, K.T., 2014. Bypassing cultivation to identify bacterial species. Microbe Magazine, 9, 111-118.

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, 2182-2192, https://doi.org/10.1038/s41467-019-10210-3.

Alanjary, M., Steinke, K. and Ziemert, N., 2019. AutoMLST: an automated web server for generating multi-locus species trees highlighting natural product potential. Nucleic Acids Research, 47(W1), 276-282, https://doi.org/10.1093/nar/gkz282.

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(W1), 29-35, https://doi.org/10.1093/nar/gkab335.

UniProt Consortium, 2019. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Research, 47(D1), D506-D515, https://doi.org/10.1093/nar/gky1049.

Hata, EM., Yusof, MT. and Zulperi, D., 2021. Induction of systemic resistance against bacterial leaf streak disease and growth promotion in rice plant by Streptomyces shenzhenesis TKSC3 and Streptomyces sp. SS8. The Plant Pathology Journal, 37, 173-181, https://doi.org/10.5423/ppj.oa.05.2020.0083.

Mahmoud, A.-L.E. and Abd-Alla, M.H., 2001. Siderophore production by some microorganisms and their effect on Bradyrhizobium-Mung Bean symbiosis. International Journal of Chemical Studies, 3, 157-162.

Nonomura, H. and Ohara, Y., 1960. Distribution of actinomycetes in soil. IV. The isolation and classification of the genus Microbispora. Journal of Fermentation Technology, 38, 401-405.

Konstantinidis, K.T., Rosselló-Móra, R. and Amann, R., 2017. Uncultivated microbes in need of their own taxonomy. The ISME Journal, 11, 2399-2406, https://doi.org/10.1038/ismej.2017.113.

Goris, J., Konstantinidis, K.T., Klappenbach, J.A., Coenye, T., Vandamme, P. and Tiedje, J.M., 2007. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. International Journal of Systematic and Evolutionary Microbiology, 57, 81-91, https://doi.org/10.1099/ijs.0.64483-0.

Rodriguez, H. and Fraga, R., 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnology Advances, 17(4-5), 31-39, https://doi.org/10.1016/S0734-9750(99)00014-2.

Carro, L. and Nouioui, I., 2017. Taxonomy and systematics of plant probiotic bacteria in the genomic era. AIMS Microbiology, 3(3), 383-412.

Arshad, M. and Frankenberger, Jr. W.T., 1991. Microbial production of plant hormones. Plant and Soil, 133, 1-8, https://doi.org/10.1007/BF00011893.

Ouyang, J., Shao, X. and Li, J., 2000. Indole-3-glycerol phosphate, a branchpoint of indole-3-acetic acid biosynthesis from the tryptophan biosynthetic pathway in Arabidopsis thaliana. The Plant Journal for Cell and Molecular Biology, 24(3), 327-333, https://doi.org/10.1046/j.1365-313x.2000.00883.x.

Lambrecht, J.A. and Downs, D.M., 2013. Anthranilate phosphoribosyl transferase (TrpD) generates phosphoribosylamine for thiamine synthesis from enamines and phosphoribosyl pyrophosphate. ACS Chemical Biology, 8(1), 242-248, https://doi.org/10.1021/cb300364k.

Calvo, P., Nelson, L. and Kloepper, J.W., 2014. Agricultural uses of plant biostimulants. Plant and Soil, 383, 3-41, https://doi.org/10.1007/s11104-014-2131-8.

Müller, W.E.G., Schröder, H.C. and Wang, X., 2019. Inorganic polyphosphates as storage for and generator of metabolic energy in the extracellular matrix. Chemical Reviews, 119, 12337-12374, https://doi.org/10.1021/acs.chemrev.9b00460.

Willsky, G.R. and Malamy, M.H., 1980. Characterization of two genetically separable inorganic phosphate transport systems in Escherichia coli. Journal of Bacteriology, 144, 356-365, https://doi.org/10.1128/jb.144.1.356-365.1980.

Carroll, C.S. and Moore, M.M., 2018. Ironing out siderophore biosynthesis: a review of non-ribosomal peptide synthetase (NRPS)-independent siderophore synthetases. Critical Reviews in Biochemistry and Molecular Biology, 53(4), 356-381, https://doi.org/10.1080/10409238. 2018.1476449.

Lee, G.C., Lee, Y.J., Kim., B.S., Kim, M.J., Nam, S., Oh, S.A., Kim, Y.S., Choi, I. and Park, J.G., 2014. Molecular characterization of actinomycetes isolated from terrestrial environment and their synthesis of geosmin and 2-MIB. Journal of Pure and Applied Microbiology, 8, 103-113.

Zabolotneva, A.A., Shatova, O.P., Sadova, A.A., Shestopalov, A.V. and Roumiantsev S.A., 2022. An overview of alkylresorcinols biological properties and effects. Journal of Nutrition and Metabolism, 2022, https://doi.org/10.1155%2F2022%2F4667607.

Pan, G., Xu, Z., Guo, Z., Hindra, Ma, M., Yang, D., Zhou, H., Gansemans, Y., Zhu, X., Huang, Y., Zhao, L.-X., Jiang, Y., Cheng, J., Van Nieuwerburgh, F., Suh, J.-W., Duan, Y. and Shen, B., 2017. Discovery of the leinamycin family of natural products by mining actinobacterial genomes. Proceedings of the National Academy of Sciences of the United States of America, 114(52), E11131-E11140, https://doi.org/10.1073/pnas.1716245115.

Fang, Y.-L., Cui, Y., Zhou, L., Thawai, C., Naqvi, T.A., Zhang, H.Y. and He, Y.-W., 2021. H-NS family protein MvaU downregulates phenazine-1-carboxylic acid (PCA) biosynthesis via binding to an AT-rich region within the promoter of the phz2 gene cluster in the rhizobacterium Pseudomonas strain PA1201. Synthetic and Systems Biotechnology, 6(4), 262-271, https://doi.org/10.1016/j.synbio.2021.09.006.

Zhao, W., Peng, F., Wang, C.-X., Yang, X., Lin, R., Fang, Z.-K., Sun, F., Lian, Y.-Y. and Jiang, H., 2020. FW0622, a new siderophore isolated from marine Verrucosispora sp. by genomic mining. Natural Product Research, 34(21), 3082-3088, https://doi.org/10.1080/

2019.1608541.

Bunbamrung, N., Kittisrisopit, S., Intaraudom, C., Dramae, A., Thawai, C., Niemhom, N., Harding, D.J., Auncharoen, P. and Pittayakhajonwut, P., 2021. Abyssomicin derivatives from the rhizosphere soil actinomycete Microbispora rhizosphaerae sp. nov. TBRC6028. Phytochemistry, 185, 1-7, https://doi.org/10.1016/j.phytochem.2021.112700.