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Effect of Bacillus mesonae H20-5 Treatment on Rhizospheric Bacterial Community of Tomato Plants under Salinity Stress

  • Lee, Shin Ae (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Kim, Hyeon Su (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Sang, Mee Kyung (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Song, Jaekyeong (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration) ;
  • Weon, Hang-Yeon (Agricultural Microbiology Division, National Institute of Agricultural Sciences, Rural Development Administration)
  • Received : 2021.10.21
  • Accepted : 2021.11.21
  • Published : 2021.12.01

Abstract

Plant growth-promoting bacteria improve plant growth under abiotic stress conditions. However, their effects on microbial succession in the rhizosphere are poorly understood. In this study, the inoculants of Bacillus mesonae strain H20-5 were administered to tomato plants grown in soils with different salinity levels (EC of 2, 4, and 6 dS/m). The bacterial communities in the bulk and rhizosphere soils were examined 14 days after H20-5 treatment using Illumina MiSeq sequencing of the bacterial 16S rRNA gene. Although the abundance of H20-5 rapidly decreased in the bulk and rhizosphere soils, a shift in the bacterial community was observed following H20-5 treatment. The variation in bacterial communities due to H20-5 treatment was higher in the rhizosphere than in the bulk soils. Additionally, the bacterial species richness and diversity were greater in the H20-5 treated rhizosphere than in the control. The composition and structure of the bacterial communities varied with soil salinity levels, and those in the H20-5 treated rhizosphere soil were clustered. The members of Actinobacteria genera, including Kineosporia, Virgisporangium, Actinoplanes, Gaiella, Blastococcus, and Solirubrobacter, were enriched in the H20-5 treated rhizosphere soils. The microbial co-occurrence network of the bacterial community in the H20-5 treated rhizosphere soils had more modules and keystone taxa compared to the control. These findings revealed that the strain H20-5 induced systemic tolerance in tomato plants and influenced the diversity, composition, structure, and network of bacterial communities. The bacterial community in the H20-5 treated rhizosphere soils also appeared to be relatively stable to soil salinity changes.

Keywords

Acknowledgement

This research was carried out with the support of "Cooperative Research Program for Agricultural Science & Technology Development (Project No. PJ01424401)", Rural Development Administration, South Korea.

References

  1. Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26:32-46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
  2. Antoun, H., Beauchamp, C. J., Goussard, N., Chabot, R. and Lalande, R. 1998. Potential of Rhizobium and Bradyrhizobium species as plant growth promoting rhizobacteria on nonlegumes: effect on radishes (Raphanus sativus L.). Plant Soil 204:57-67. https://doi.org/10.1023/A:1004326910584
  3. Backer, R., Rokem, J. S., Ilangumaran, G., Lamont, J., Praslickova, D., Ricci, E., Subramanian, S. and Smith, D. L. 2018. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 9:1473. https://doi.org/10.3389/fpls.2018.01473
  4. Bulgarelli, D., Schlaeppi, K., Spaepen, S., Ver Loren van Themaat, E. and Schulze-Lefert, P. 2013. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64:807-838. https://doi.org/10.1146/annurev-arplant-050312-120106
  5. Carvalhais, L. C., Dennis, P. G., Badri, D. V., Tyson, G. W., Vivanco, J. M. and Schenk, P. M. 2013. Activation of the jasmonic acid plant defence pathway alters the composition of rhizosphere bacterial communities. PLoS ONE 8:e56457. https://doi.org/10.1371/journal.pone.0056457
  6. Casamayor, E. O., Massana, R., Benlloch, S., Ovreas, L., Diez, B., Goddard, V. J., Gasol, J. M., Joint, I., Rodriguez-Valera, F. and Pedros-Alio, C. 2002. Changes in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multipond solar saltern. Environ. Microbiol. 4:338-348. https://doi.org/10.1046/j.1462-2920.2002.00297.x
  7. Chaparro, J. M., Badri, D. V. and Vivanco, J. M. 2014. Rhizosphere microbiome assemblage is affected by plant development. ISME J. 8:790-803. https://doi.org/10.1038/ismej.2013.196
  8. Clarke, K. R. 1993. Nonparametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117-143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
  9. Cole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y., Brown, C. T., Porras-Alfaro, A., Kuske, C. R. and Tiedje, J. M. 2014. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42:D633-D642. https://doi.org/10.1093/nar/gkt1244
  10. Compant, S., Samad, A., Faist, H. and Sessitsch, A. 2019. A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J. Adv. Res. 19:29-37. https://doi.org/10.1016/j.jare.2019.03.004
  11. De Caceres, M. and Legendre, P. 2009. Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566-3574. https://doi.org/10.1890/08-1823.1
  12. Deng, Y., Jiang, Y.-H., Yang, Y., He, Z., Luo, F. and Zhou, J. 2012. Molecular ecological network analyses. BMC Bioinform. 13:113. https://doi.org/10.1186/1471-2105-13-113
  13. Edgar, R. C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10:996-998. https://doi.org/10.1038/nmeth.2604
  14. Edwards, J., Johnson, C., Santos-Medellin, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., Eisen, J. A. and Sundaresan, V. 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. U. S. A. 112:E911-E920.
  15. Edwards, J. A., Santos-Medellin, C. M., Liechty, Z. S., Nguyen, B., Lurie, E., Eason, S., Phillips, G. and Sundaresan, V. 2018. Compositional shifts in root-associated bacterial and archaeal microbiota track the plant life cycle in field-grown rice. PLoS Biol. 16:e2003862. https://doi.org/10.1371/journal.pbio.2003862
  16. Gadhave, K. R., Devlin, P. F., Ebertz, A., Ross, A. and Gange, A. C. 2018. Soil inoculation with Bacillus spp. modifies root endophytic bacterial diversity, evenness, and community composition in a context-specific manner. Microb. Ecol. 76:741-750. https://doi.org/10.1007/s00248-018-1160-x
  17. Garbeva, P., van Veen, J. A. and van Elsas, J. D. 2004. Microbial diversity in soil: selection microbial populations by plant and soil type and implications for disease suppressiveness. Annu. Rev. Phytopathol. 42:243-270. https://doi.org/10.1146/annurev.phyto.42.012604.135455
  18. Glick, B. R. 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:963401. https://doi.org/10.6064/2012/963401
  19. Jamil, A., Riaz, S., Ashraf, M. and Foolad, M. R. 2011. Gene expression profiling of plants under salt stress. Crit. Rev. Plant Sci. 30:435-458. https://doi.org/10.1080/07352689.2011.605739
  20. Kim, J. M., Roh, A.-S., Choi, S.-C., Kim, E.-J., Choi, M.-T., Ahn, B.-K., Kim, S.-K., Lee, Y.-H., Joa, J.-H., Kang, S.-S., Lee, S. A., Ahn, J.-H., Song, J. and Weon, H.-Y. 2016. Soil pH and electrical conductivity are key edaphic factors shaping bacterial communities of greenhouse soils in Korea. J. Microbiol. 54:838-845. https://doi.org/10.1007/s12275-016-6526-5
  21. Lebeis, S. L., Paredes, S. H., Lundberg, D. S., Breakfield, N., Gehring, J., McDonald, M., Malfatti, S., Glavina del Rio, T., Jones, C. D., Tringe, S. G. and Dangl, J. L. 2015. PLANT MICROBIOME: salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860-864. https://doi.org/10.1126/science.aaa8764
  22. Lee, S. A., Kim, Y., Kim, J. M., Chu, B., Joa, J.-H., Sang, M. K., Song, J. and Weon, H.-Y. 2019. A preliminary examination of bacterial, archaeal, and fungal communities inhabiting different rhizocompartments of tomato plants under real-world environments. Sci. Rep. 9:9300. https://doi.org/10.1038/s41598-019-45660-8
  23. Legendre, P. and Gallagher, E. D. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129:271-280. https://doi.org/10.1007/s004420100716
  24. Liu, H., Carvalhais, L. C., Schenk, P. M. and Dennis, P. G. 2017. Effects of jasmonic acid signalling on the wheat microbiome differ between body sites. Sci. Rep. 7:41766. https://doi.org/10.1038/srep41766
  25. Liu, H., Xiong, W., Zhang, R., Hang, X., Wang, D., Li, R. and Shen, Q. 2018. Continuous application of different organic additives can suppress tomato disease by inducing the healthy rhizospheric microbiota through alterations to the bulk soil microflora. Plant Soil 423:229-240. https://doi.org/10.1007/s11104-017-3504-6
  26. Masciarelli, O., Llanes, A. and Luna, V. 2014. A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol. Res. 169:609-615. https://doi.org/10.1016/j.micres.2013.10.001
  27. Min, W., Guo, H., Zhang, W., Zhou, G., Ma, L., Ye, J., Liang, Y. and Hou, Z. 2016. Response of soil microbial community and diversity to increasing water salinity and nitrogen fertilization rate in an arid soil. Acta Agric. Scand. Sect. B Soil Plant Sci. 66:117-126. https://doi.org/10.1080/09064710.2015.1078838
  28. Mueller, L. A., Kugler, K. G., Dander, A., Graber, A. and Dehmer, M. 2011. QuACN: an R package for analyzing complex biological networks quantitatively. Bioinformatics 27:140-141. https://doi.org/10.1093/bioinformatics/btq606
  29. Munns, R. 2005. Genes and salt tolerance: bringing them together. New Phytol. 167:645-663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
  30. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. 2013. Vegan: community ecology package. R package version 2.0-10. R Foundation for Statistical Computing, Vienna, Austria.
  31. Olesen, J. M., Bascompte, J., Dupont, Y. L. and Jordano, P. 2007. The modularity of pollination networks. Proc. Natl. Acad. Sci. U. S. A. 104:19891-19896. https://doi.org/10.1073/pnas.0706375104
  32. Panke-Buisse, K., Poole, A. C., Goodrich, J. K., Ley, R. E. and Kao-Kniffin, J. 2015. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J. 9:980-989. https://doi.org/10.1038/ismej.2014.196
  33. Polonenko, D. R., Mayfield, C. I. and Dumbroff, E. B. 1986. Microbial responses to salt-induced osmotic stress. Plant Soil 92:417-425. https://doi.org/10.1007/BF02372489
  34. R Development Core Team. 2014. R: a language and environment for statistical computing. URL http://www.R-project.org/ [21 October 2021].
  35. Sawant, S. S., Kim, S. Y., Sang, M. K., Weon, H.-Y., Kim, S. and Song, J. 2019. Complete genome sequence of Bacillus mesonae H20-5, an efficient strain enhancing abiotic stress tolerance in plants. Korean J. Microbiol. 55:408-410.
  36. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J. and Weber, C. F. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. https://doi.org/10.1128/AEM.01541-09
  37. Shi, S., Nuccio, E. E., Shi, Z. J., He, Z., Zhou, J. and Firestone, M. K. 2016. The interconnected rhizosphere: high network complexity dominates rhizosphere assemblages. Ecol. Lett. 19:926-936. https://doi.org/10.1111/ele.12630
  38. Shrivastava, P. and Kumar, R. 2015. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J. Biol. Sci. 22:123-131. https://doi.org/10.1016/j.sjbs.2014.12.001
  39. Tao, C., Li, R., Xiong, W., Shen, Z., Liu, S., Wang, B., Ruan, Y., Geisen, S., Shen, Q. and Kowalchuk, G. A. 2020. Bio-organic fertilizers stimulate indigenous soil Pseudomonas populations to enhance plant disease suppression. Microbiome 8:137. https://doi.org/10.1186/s40168-020-00892-z
  40. Toju, H., Peay, K. G., Yamamichi, M., Narisawa, K., Hiruma, K., Naito, K., Fukuda, S., Ushio, M., Nakaoka, S., Onoda, Y., Yoshida, K., Schlaeppi, K., Bai, Y., Sugiura, R., Ichihashi, Y., Minamisawa, K. and Kiers, E. T. 2018. Core microbiomes for sustainable agroecosystems. Nat. Plants 4:247-257. https://doi.org/10.1038/s41477-018-0139-4
  41. Trabelsi, D. and Mhamdi, R. 2013. Microbial inoculants and their impact on soil microbial communities: a review. Biomed. Res. Int. 2013:863240.
  42. Wang, L., Lu, X., Yuan, H., Wang, B. and Shen, Q. 2015. Application of bio-organic fertilizer to control tomato fusarium wilting by manipulating soil microbial communities and development. Commun. Soil Sci. Plant Anal. 46:2311-2322. https://doi.org/10.1080/00103624.2015.1081694
  43. Wang, Q., Garrity, G. M., Tiedje, J. M. and Cole, J. R. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267. https://doi.org/10.1128/AEM.00062-07
  44. Wei, Z., Gu, Y., Friman, V.-P., Kowalchuk, G. A., Xu, Y., Shen, Q. and Jousset, A. 2019. Initial soil microbiome composition and functioning predetermine future plant health. Sci. Adv. 5:eaaw0759. https://doi.org/10.1126/sciadv.aaw0759
  45. Xue, C., Penton, C. R., Shen, Z., Zhang, R., Huang, Q., Li, R., Ruan, Y. and Shen, Q. 2015. Manipulating the banana rhizosphere microbiome for biological control of Panama disease. Sci. Rep. 5:11124. https://doi.org/10.1038/srep11124
  46. Yang, H., Hu, J., Long, X., Liu, Z. and Rengel, Z. 2016. Salinity altered root distribution and increased diversity of bacterial communities in the rhizosphere soil of Jerusalem artichoke. Sci. Rep. 6:20687. https://doi.org/10.1038/srep20687
  47. Yang, J., Kloepper, J. W. and Ryu, C.-M. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14:1-4. https://doi.org/10.1016/j.tplants.2008.10.004
  48. Yoo, S.-J., Kim, J. W., Kim, S. T., Weon, H.-Y., Song, J. and Sang, M. K. 2019a. Effect of Bacillus mesonae H20-5 on fruit yields and quality in protected cultivation. Res. Plant Dis. 25:84-88. https://doi.org/10.5423/RPD.2019.25.2.84
  49. Yoo, S.-J., Weon, H.-Y., Song, J. and Sang, M. K. 2019b. Induced tolerance to salinity stress by halotolerant bacteria Bacillus aryabhattai H19-1 and B. mesonae H20-5 in tomato plants. J. Microbiol. Biotechnol. 29:1124-1136. https://doi.org/10.4014/jmb.1904.04026
  50. Zhang, L.-N., Wang, D.-C., Hu, Q., Dai, X.-Q., Xie, Y.-S., Li, Q., Liu, H.-M. and Guo, J.-H. 2019a. Consortium of plant growth-promoting rhizobacteria strains suppresses sweet pepper disease by altering the rhizosphere microbiota. Front. Microbiol. 10:1668. https://doi.org/10.3389/fmicb.2019.01668
  51. Zhang, Y., Gao, X., Shen, Z., Zhu, C., Jiao, Z., Li, R. and Shen, Q. 2019b. Pre-colonization of PGPR triggers rhizosphere microbiota succession associated with crop yield enhancement. Plant Soil 439:553-567. https://doi.org/10.1007/s11104-019-04055-4
  52. Zolla, G., Badri, D. V., Bakker, M. G., Manter, D. K. and Vivanco, J. M. 2013. Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl. Soil Ecol. 68:1-9. https://doi.org/10.1016/j.apsoil.2013.03.007