Rhizocompartments and environmental factors affect microbial composition and variation in native plants

Abstract

Molecular analysis based on large-scale sequencing of the plant microbiota has revealed complex relationships between plants and microbial communities, and environmental factors such as soil type can influence these relationships. However, most studies on root-associated microbial communities have focused on model plants such as Arabidopsis, rice or crops. Herein, we examined the microbiota of rhizocompartments of two native plants, Sedum takesimense Nakai and Campanula takesimana Nakai, using archaeal and bacterial 16S rRNA gene amplicon profiling, and assessed relationships between environmental factors and microbial community composition. We identified 390 bacterial genera, including known plant-associated genera such as Pseudomonas, Flavobacterium, Bradyrhizobium and Rhizobium, and uncharacterized clades such as DA101 that might be important in root-associated microbial communities in bulk soil. Unexpectedly, Nitrososphaera clade members were abundant, indicating functional association with roots. Soil texture/type has a greater impact on microbial community composition in rhizocompartments than chemical factors. Our results provide fundamental knowledge on microbial diversity, community and correlations with environmental factors, and expand our understanding of the microbiota in rhizocompartments of native plants.

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References

  1. Alonso, C., Warnecke, F., Amann, R., and Pernthaler, J. 2007. High local and global diversity of Flavobacteria in marine plankton. Environ. Microbiol. 9, 1253–1266.

    Article  CAS  PubMed  Google Scholar 

  2. Baltrus, D.A. 2017. Adaptation, specialization, and coevolution within phytobiomes. Curr. Opin. Plant Biol. 38, 109–116.

    Article  PubMed  Google Scholar 

  3. Berendsen, R.L., Pieterse, C.M., and Bakker, P.A. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486.

    Article  CAS  PubMed  Google Scholar 

  4. Bernardet, J.F. and Bowman, J.P. 2006. The genu. Flavobacterium, pp. 481–531. In Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.H., and Stackebrandt, E. (eds.), The prokaryotes: Volume 7: Proteobacteria: Delta, epsilon subclass. Springer New York, New York, NY, USA.

    Google Scholar 

  5. Bever, J.D. 1994. Feeback between plants and their soil communities in an old field community. Ecology 75, 1965–1977.

    Article  Google Scholar 

  6. Bhullar, G.S., Edwards, P.J., and Olde Venterink, H. 2014. Influence of different plant species on methane emissions from soil in a restored Swiss wetland. PLoS One 9, e89588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bodenhausen, N., Horton, M.W., and Bergelson, J. 2013. Bacterial communities associated with the leaves and the roots o. Arabidopsis thaliana. PLoS One 8, e56329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Breidenbach, B. and Conrad, R. 2014. Seasonal dynamics of bacterial and archaeal methanogenic communities in flooded rice fields and effect of drainage. Front. Microbiol. 5, 752.

    PubMed  Google Scholar 

  9. Breidenbach, B., Pump, J., and Dumont, M.G. 2015. Microbial community structure in the rhizosphere of rice plants. Front. Microbiol. 6, 1537.

    PubMed  Google Scholar 

  10. Brewer, T.E., Handley, K.M., Carini, P., Gilbert, J.A., and Fierer, N. 2016. Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’. Nat. Microbiol. 2, 16198.

    Article  CAS  PubMed  Google Scholar 

  11. Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E.. et al. 2012. Revealing structure and assembly cues fo. Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95.

    Article  CAS  PubMed  Google Scholar 

  12. 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.

    Article  CAS  PubMed  Google Scholar 

  13. Burt, R., United, S., Natural Resources Conservation, S., National Soil Survey, C., and National Soil Survey, L. 2004. Soil survey laboratory methods manual. United States dept. of agriculture, Natural resources conservation service, Washington, D.C., USA.

    Google Scholar 

  14. Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S.M., Betley, J., Fraser, L., Bauer, M.. et al. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Chaparro, J.M., Badri, D.V., and Vivanco, J.M. 2014. Rhizosphere microbiome assemblage is affected by plant development. ISME J. 8, 790–803.

    Article  CAS  PubMed  Google Scholar 

  16. Choi, H., Koh, H. W., Kim, H., Chae, J. C., and Park, S.J. 2016. Microbial community composition in the marine sediments of Jeju Island: Next-generation sequencing surveys. J. Microbiol. Biotechnol. 26, 883–890.

    Article  CAS  PubMed  Google Scholar 

  17. Coleman-Derr, D., Desgarennes, D., Fonseca-Garcia, C., Gross, S., Clingenpeel, S., Woyke, T., North, G., Visel, A., Partida-Martinez, L.P., and Tringe, S.G. 2016. Plant compartment and biogeography affect microbiome composition in cultivated and nativ. Agave species. New Phytol. 209, 798–811.

    Article  CAS  PubMed  Google Scholar 

  18. Debenport, S.J., Assigbetse, K., Bayala, R., Chapuis-Lardy, L., Dick, R.P., and McSpadden Gardener, B.B. 2015. Association of shifting populations in the root zone microbiome of millet with enhanced crop productivity in the Sahel region (Africa). Appl. Environ. Microbiol. 81, 2841–2851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 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. USA 112, E911–920.

    Article  CAS  PubMed  Google Scholar 

  20. Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783–791.

    Article  Google Scholar 

  21. Harrell, F.E. Jr., with contributions from Charles Dupont and many others. 2018. Hmisc: Harrell Miscellaneous. R package version 4.1-1. https://doi.org/CRAN.R-project.org/package=Hmisc.

    Google Scholar 

  22. Hartmann, A., Rothballer, M., and Schmid, M. 2008. Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312, 7–14.

    Article  CAS  Google Scholar 

  23. Jahn, R., Blume, H.P., Asio, V.B., Spaargaren, O., and Schad, P. 2006. Guidelines for soil description, 4th edition. FAO, Rome, Italy.

    Google Scholar 

  24. Jung, S.Y., Byun, J.G., Park, S.H., Oh, S.H., Yang, J.C., Jang, J.W., Chang, K.S., and Lee, Y.M. 2014. The study of distribution characteristics of vascular and naturalized plants in Dokdo, South Korea. J. Asia Pac. Biodivers. 7, e197–e205.

    Article  Google Scholar 

  25. Knaebel, D.B., Federle, T.W., McAvoy, D.C., and Vestal, J.R. 1994. Effect of mineral and organic soil constituents on microbial mineralization of organic compounds in a natural soil. Appl. Environ. Microbiol. 60, 4500–4508.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Kolton, M., Sela, N., Elad, Y., and Cytryn, E. 2013. Comparative genomic analysis indicates that niche adaptation of terrestria. Flavobacteria is strongly linked to plant glycan metabolism. PLoS One 8, e76704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kong, Y., Kong, J., Wang, D., Huang, H., Geng, K., Wang, Y., and Xia, Y. 2017. Effect o. Ageratina adenophora invasion on the composition and diversity of soil microbiome. J. Gen. Appl. Microbiol. 63, 114–121.

    Article  CAS  PubMed  Google Scholar 

  28. Koyama, A., Steinweg, J.M., Haddix, M.L., Dukes, J.S., and Wallenstein, M.D. 2018. Soil bacterial community responses to altered precipitation and temperature regimes in an old field grassland are mediated by plants. FEMS Microbiol. Ecol. 94, fix156.

  29. Kumar, S., Stecher, G., and Tamura, K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.

    Article  CAS  PubMed  Google Scholar 

  30. Kwak, M.J., Kong, H.G., Choi, K., Kwon, S.K., Song, J.Y., Lee, J., Lee, P.A., Choi, S.Y., Seo, M., Lee, H.J.. et al. 2018. Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat. Biotechnol. 36, 1100–1109.

    Article  CAS  Google Scholar 

  31. Lee, G.S. and Choo, Y.S. 2009. Physical and chemical characteristics of Dokdo soil. J. Ecol. Environ. 32, 295–304.

    Article  Google Scholar 

  32. Lugtenberg, B. and Kamilova, F. 2009. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556.

    Article  CAS  PubMed  Google Scholar 

  33. Lundberg, D.S., Lebeis, S.L., Paredes, S.H., Yourstone, S., Gehring, J., Malfatti, S., Tremblay, J., Engelbrektson, A., Kunin, V., Del Rio, T.G.. et al. 2012. Defining the cor. Arabidopsis thaliana root microbiome. Nature 488, 86–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mamet, S.D., Lamb, E.G., Piper, C.L., Winsley, T., and Siciliano, S.D. 2017. Archaea and bacteria mediate the effects of native species root loss on fungi during plant invasion. ISME J. 11, 1261–1275.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Mendes, R., Garbeva, P., and Raaijmakers, J.M. 2013. The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev. 37, 634–663.

    Article  CAS  PubMed  Google Scholar 

  36. Nayak, D.R., Babu, Y.J., Datta, A., and Adhya, T.K. 2007. Methane oxidation in an intensively cropped tropical rice field soil under long-term application of organic and mineral fertilizers. J. Environ. Qual. 36, 1577–1584.

    Article  CAS  PubMed  Google Scholar 

  37. Naylor, D., DeGraaf, S., Purdom, E., and Coleman-Derr, D. 2017. Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J. 11, 2691–2704.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Pinton, R., Varanini, Z., and Nannipieri, P. 2007. The rhizosphere: Biochemistry and organic substances at the soil-plant interface, second edition. CRC Press.

    Google Scholar 

  39. Poulsen, M., Schwab, C., Jensen, B.B., Engberg, R.M., Spang, A., Canibe, N., Hojberg, O., Milinovich, G., Fragner, L., Schleper, C.. et al. 2013. Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat. Commun. 4, 1428.

    Article  CAS  PubMed  Google Scholar 

  40. Preston, G.M. 2004. Plant perceptions of plant growth-promotin. Pseudomonas. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359, 907–918.

    Article  CAS  PubMed  Google Scholar 

  41. Rani, S., Koh, H.W., Rhee, S.K., Fujitani, H., and Park, S.J. 2017. Detection and diversity of the nitrite oxidoreductase alpha subunit (nxrA) gene o. Nitrospina in marine sediments. Microb. Ecol. 73, 111–122.

    Article  CAS  PubMed  Google Scholar 

  42. Reysenbach, A.L. 2015. Thermoplasmata class. nov. In. Bergey’s manual of systematics of archaea and bacteria. John Wiley & Sons, Ltd.

    Google Scholar 

  43. Sangwan, P., Kovac, S., Davis, K.E., Sait, M., and Janssen, P.H. 2005. Detection and cultivation of soil verrucomicrobia. Appl. Environ. Microbiol. 71, 8402–8410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Schlaeppi, K. and Bulgarelli, D. 2015. The plant microbiome at work. Mol. Plant Microbe Interact. 28, 212–217.

    Article  CAS  PubMed  Google Scholar 

  45. Schloss, P.D., Gevers, D., and Westcott, S.L. 2011. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6, e27310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Schreiter, S., Ding, G.C., Heuer, H., Neumann, G., Sandmann, M., Grosch, R., Kropf, S., and Smalla, K. 2014. Effect of the soil type on the microbiome in the rhizosphere of field-grown lettuce. Front. Microbiol. 5, 144.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Shoji, S., Nanzyo, M., and Dahlgren, R.A. 1994. Volcanic ash soils: Genesis, properties and utilization. Elsevier science.

    Google Scholar 

  49. Song, G.C., Im, H., Jung, J., Lee, S., Jung, M.Y., Rhee, S.K., and Ryu, C.M. 2018. Plant growth-promoting archaea trigger induced systemic resistance i. Arabidopsis thaliana agains. Pectobacterium carotovorum an. Pseudomonas syringae. Environ. Microbiol. 21, 940–948.

    Article  CAS  Google Scholar 

  50. Sun, B.Y., Sul, M.R., Im, J.A., Kim, C.H., and Kim, T.J. 2002. Evolution of endemic vascular plants of Ulleungdo and Dokdo in Korea - floristic and cytotaxonomic characteristics of vascular flora of Dokdo. Korean J. Plant Taxon. 32, 143–158.

    Article  Google Scholar 

  51. Thomas, F. and Cebron, A. 2016. Short-term rhizosphere effect on available carbon sources, phenanthrene degradation, and active microbiome in an aged-contaminated industrial soil. Front. Microbiol. 7, 92.

    PubMed  PubMed Central  Google Scholar 

  52. Vetriani, C., Jannasch, H.W., MacGregor, B.J., Stahl, D.A., and Reysenbach, A.L. 1999. Population structure and phylogenetic characterization of marine benthic archaea in deep-sea sediments. Appl. Environ. Microbiol. 65, 4375–4384.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Wagner, M.R., Lundberg, D.S., Coleman-Derr, D., Tringe, S.G., Dangl, J.L., and Mitchell-Olds, T. 2014. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wil. Arabidopsis relative. Ecol. Lett. 17, 717–726.

    Article  PubMed  Google Scholar 

  54. Whiteside, S.A., Razvi, H., Dave, S., Reid, G., and Burton, J.P. 2015. The microbiome of the urinary tract-a role beyond infection. Nat. Rev. Urol. 12, 81–90.

    Article  PubMed  Google Scholar 

  55. Yeoh, Y.K., Dennis, P.G., Paungfoo-Lonhienne, C., Weber, L., Brackin, R., Ragan, M.A., Schmidt, S., and Hugenholtz, P. 2017. Evolutionary conservation of a core root microbiome across plant phyla along a tropical soil chronosequence. Nat. Commun. 8, 215.

  56. Zhang, H., Sun, Y., Xie, X., Kim, M.S., Dowd, S.E., and Pare, P.W. 2009. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J. 58, 568–577.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by funds to SJP from the Basic Research Program, funded by the National Research Foundation of Korea (no. 2018R1C1B6006762), and the National Institute of Biological Resources, funded by the Ministry of Environment (no. NIBR201701107 and NIBR201835102).

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Correspondence to Soo-Je Park.

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Kang, MS., Hur, M. & Park, SJ. Rhizocompartments and environmental factors affect microbial composition and variation in native plants. J Microbiol. 57, 550–561 (2019). https://doi.org/10.1007/s12275-019-8646-1

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Keywords

  • plant microbiota
  • rhizocompartments
  • environmental factors
  • next-generation sequencing
  • archaea
  • bacteria