Skip to main content

Advertisement

Log in

Nicotiana Roots Recruit Rare Rhizosphere Taxa as Major Root-Inhabiting Microbes

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Root-associated microbes have a profound impact on plant health, yet little is known about the distribution of root-associated microbes among different root morphologies or between rhizosphere and root environments. We explore these issues here with two commercial varieties of burley tobacco (Nicotiana tabacum) using 16S rRNA gene amplicon sequencing from rhizosphere soil, as well as from primary, secondary, and fine roots. While rhizosphere soils exhibited a fairly rich and even distribution, root samples were dominated by Proteobacteria. A comparison of abundant operational taxonomic units (OTUs) between rhizosphere and root samples indicated that Nicotiana roots select for rare taxa (predominantly Proteobacteria, Verrucomicrobia, Actinobacteria, Bacteroidetes, and Acidobacteria) from their corresponding rhizosphere environments. The majority of root-inhabiting OTUs (~80 %) exhibited habitat generalism across the different root morphological habitats, although habitat specialists were noted. These results suggest a specific process whereby roots select rare taxa from a larger community.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Bardgett RD, Mommer L, De Vries FT (2014) Going underground: root traits as drivers of ecosystem processes. Trends Ecol Evol 29:692–699. doi:10.1016/j.tree.2014.10.006

    Article  PubMed  Google Scholar 

  2. Meister R, Rajani MS, Ruzicka D, Schachtman DP (2014) Challenges of modifying root traits in crops for agriculture. Trends Plant Sci 19:779–788. doi:10.1016/j.tplants.2014.08.005

    Article  CAS  PubMed  Google Scholar 

  3. Parker JS, Cavell AC, Dolan L et al (2000) Genetic interactions during root hair morphogenesis in Arabidopsis. Plant Cell 12:1961–1974. doi:10.1105/tpc.12.10.1961

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Smith S, Smet ID (2012) Root system architecture: insights from Arabidopsis and cereal crops. Philos Trans R Soc London Ser B 367:1441–1452. doi:10.1098/rstb.2011.0234

    Article  CAS  Google Scholar 

  5. Lebeis SL (2015) Greater than the sum of their parts: characterizing plant microbiomes at the community-level. Curr Opin Plant Biol 24:82–86. doi:10.1016/j.pbi.2015.02.004

    Article  CAS  PubMed  Google Scholar 

  6. Szoboszlay M, Lambers J, Chappell J, Kupper JV, Moe LA, McNear DH (2015) Comparison of root system architecture and rhizosphere microbial communities of Balsas teosinte and domesticated corn cultivars. Soil Biol Biochem 80:34–44. doi:10.1016/j.soilbio.2014.09.001

    Article  CAS  Google Scholar 

  7. Saleem M, Moe LA (2014) Multitrophic microbial interactions for eco- and agro-biotechnological processes: theory and practice. Trends Biotechnol 32:529–537. doi:10.1016/j.tibtech.2014.08.002

    Article  CAS  PubMed  Google Scholar 

  8. terHorst CP, Lennon JT, Lau JA (2014) The relative importance of rapid evolution for plant-microbe interactions depends on ecological context. Philos Trans R Soc London Ser B 281:20140028. doi:10.1098/rspb.2014.0028

    Article  Google Scholar 

  9. Ikeda S, Kaneko T, Okubo T et al (2009) Development of a bacterial cell enrichment method and its application to the community analysis in soybean stems. Microb Ecol 58:703–714. doi:10.1007/s00248-009-9566-0

    Article  CAS  PubMed  Google Scholar 

  10. Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. doi:10.1128/AEM.01043-13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95. doi:10.1038/nature11336

    Article  CAS  PubMed  Google Scholar 

  12. Lundberg DS, Lebeis SL, Paredes SH et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. doi:10.1038/nature11237

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Schlaeppi K, Dombrowski N, Oter RG et al (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. PNAS 111:585–592. doi:10.1073/pnas.1321597111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Ofek-Lalzar M, Sela N, Goldman-Voronov M et al (2014) Niche and host-associated functional signatures of the root surface microbiome. Nat Commun 5:4950. doi:10.1038/ncomms5950

    Article  CAS  PubMed  Google Scholar 

  15. DeAngelis KM, Brodie EL, DeSantis TZ et al (2008) Selective progressive response of soil microbial community to wild oat roots. ISME J 3:168–178. doi:10.1038/ismej.2008.103

    Article  PubMed  Google Scholar 

  16. Bouffaud M-L, Poirier M-A, Muller D, Moënne-Loccoz Y (2014) Root microbiome relates to plant host evolution in maize and other Poaceae. Environ Microbiol 16:2804–2814. doi:10.1111/1462-2920.12442

    Article  PubMed  Google Scholar 

  17. Fierer N, Lauber CL, Ramirez KS et al (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. doi:10.1038/ismej.2011.159

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Walke JB, Becker MH, Loftus SC et al (2014) Amphibian skin may select for rare environmental microbes. ISME J 8:2207–2217. doi:10.1038/ismej.2014.77

    Article  CAS  PubMed  Google Scholar 

  19. Ainsworth TD, Krause L, Bridge T et al (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. doi:10.1038/ismej.2015.39

    Google Scholar 

  20. Crump BC, Amaral-Zettler LA, Kling GW (2012) Microbial diversity in arctic freshwaters is structured by inoculation of microbes from soils. ISME J 6:1629–1639. doi:10.1038/ismej.2012.9

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Gaiero JR, McCall CA, Thompson KA et al (2013) Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot 100:1738–1750. doi:10.3732/ajb.1200572

    Article  PubMed  Google Scholar 

  22. Garbeva P, Overbeek LS, Vuurde JWL, Elsas JD (2001) Analysis of endophytic bacterial communities of potato by plating and denaturing gradient gel electrophoresis (DGGE) of 16S rDNA based PCR fragments. Microb Ecol 41:369–383. doi:10.1007/s002480000096

    Article  CAS  PubMed  Google Scholar 

  23. Lynch MDJ, Neufeld JD (2015) Ecology and exploration of the rare biosphere. Nat Rev Microbiol 13:217–229. doi:10.1038/nrmicro3400

    Article  CAS  PubMed  Google Scholar 

  24. Mackenzie BW, Waite DW, Taylor MW (2015) Evaluating variation in human gut microbiota profiles due to DNA extraction method and inter-subject differences. Front Microbiol, 6. doi: 10.3389/fmicb.2015.00130

Download references

Acknowledgments

We thank Colin Fisher and Anne Jack for their help in sampling and sharing the soil analysis data. We also thank Cathy Bowers for help in photography.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luke A. Moe.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 15 kb)

ESM 2

(DOCX 41.2 kb)

ESM 3

(PPTX 905 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saleem, M., Law, A.D. & Moe, L.A. Nicotiana Roots Recruit Rare Rhizosphere Taxa as Major Root-Inhabiting Microbes. Microb Ecol 71, 469–472 (2016). https://doi.org/10.1007/s00248-015-0672-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0672-x

Keywords

Navigation