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Two grass species fail to display differing species-specific effects on soil bacterial community structures after one season of greenhouse growth

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Abstract

Background and aims

Plant impacts on soil microbial community composition and function are believed to be important but remain poorly understood. We looked at the bacterial community effects of growing two different plant species in soils with differing plant growth histories.

Methods

Big bluestem (Andropogon gerardii: Ag) and cereal rye (Secale cereale: Sc) plants were grown in six soils with different planting and management histories for 14 weeks in a greenhouse study. Both prior to planting and harvesting, soil was collected for analysis. Bacterial community DNA was extracted and analyzed via 454 pyrosequencing and soil edaphic characteristics were also measured.

Results

Significant shifts in composition were observed between pre-plant and post-plant bacterial communities in 23 of the 40 most abundant orders but only one order (Nitrospirales) differed significantly between the two plant species treatments (Ag vs. Sc). Compared to pre-plant communities, post-plant communities increased significantly in alpha diversity (within community) but exhibited an overall decrease in beta diversity (between community), indicating that soil communities became more similar after growth of either Ag or Sc. Soil pH was the strongest predictor of bacterial community ordination, followed by percent carbon, organic matter, phosphorous, nitrogen, and potassium.

Conclusions

Overall, the relative lack of significant differences between the soil bacterial communities of Ag- and Sc-planted soils suggests that potential plant-species-specific effects are strongly modulated by growth conditions and edaphic soil characteristics.

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References

  • Barnes JP, Putnam AR (1987) Role of benzoxazinones in allelopathy by rye (Secale cereale L.). J Chem Ecol 13:889–906. doi:10.1007/BF01020168

    Article  CAS  PubMed  Google Scholar 

  • Bartram AK, Lynch MDJ, Stearns JC, Moreno-Hagelsieb G, Neufeld JD (2011) Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl Environ Microbiol 77:3846–3852

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baselga A, Orme CDL (2012) betapart: an R package for the study of beta diversity. Methodol Ecol Evol 3:808–812

    Article  Google Scholar 

  • Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13

    Article  CAS  PubMed  Google Scholar 

  • Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456

    Article  PubMed  Google Scholar 

  • Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

    Article  CAS  PubMed  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2010) Colloquium Paper: Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522

    Article  PubMed Central  PubMed  Google Scholar 

  • Casper BB, Castelli JP (2007) Evaluating plant–soil feedback together with competition in a serpentine grassland. Ecol Lett 10:394–400

    Article  PubMed  Google Scholar 

  • Charlson RJ, Rodhe H (1982) Factors controlling the acidity of natural rainwater. Nature 295:683–685

    Article  CAS  Google Scholar 

  • De Mendiburu, F (2007) Agricolae: statistical procedures for agricultural research, R package version 10–3

  • Dohrmann AB, Küting M, Jünemann S, Jaenicke S, Schlüter A, Tebbe CC (2013) Importance of rare taxa for bacterial diversity in the rhizosphere of Bt- and conventional maize varieties. ISME J 7:37–49

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duineveld BM, Rosado AS, van Elsas JD, van Veen JA (1998) Analysis of the dynamics of bacterial communities in the rhizosphere of the chrysanthemum via denaturing gradient gel electrophoresis and substrate utilization patterns. Appl Environ Microbiol 64:4950–4957

    CAS  PubMed Central  PubMed  Google Scholar 

  • Duineveld BM, Kowalchuk GA, Keijzer A, van Elsas JD, van Veen JA (2001) Analysis of the bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl Environ Microbiol 67:172–178

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fang C, Radosevich M, Fuhrmann JJ (2001) Characterization of rhizosphere microbial community structure in five similar grass species using FAME and BIOLOG analyses. Soil Biol Biochem 33:679–682

    Article  CAS  Google Scholar 

  • Garbeva O, van Veen JA, van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270

    Article  CAS  PubMed  Google Scholar 

  • Garbeva O, Postma J, van Veen JA, van Elsas JD (2006) Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani. Environ Microbiol 8:233–246

    Article  CAS  PubMed  Google Scholar 

  • Garbeva P, Van Elsas J, Van Veen J (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32

    Article  CAS  Google Scholar 

  • Giller PS (1996) The diversity of soil communities, the “poor man”s tropical rainforest’. Biodivers Conserv 5:135–168

    Article  Google Scholar 

  • Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378

    Article  CAS  Google Scholar 

  • Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230

    Article  CAS  PubMed  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant Soil 248:43–59

    Article  CAS  Google Scholar 

  • İnceoğlu Ö, Al-Soud WA, Salles JF, Semenov AV, Van Elsas JD (2011) Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS One 6:e23321

    Article  PubMed Central  PubMed  Google Scholar 

  • Innes L, Hobbs P, Bardgett R (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biol Fert Soils 40:7–13

    Article  Google Scholar 

  • Kielak A, Pijl AS, Van Veen JA, Kowalchuk GA (2008) Differences in vegetation composition and plant species identity lead to only minor changes in soil-borne microbial communities in a former arable field. FEMS Microbiol Ecol 63:372–382

    Article  CAS  PubMed  Google Scholar 

  • Kinkel LL, Schlatter DC, Bakker MG, Arenz BE (2012) Streptomyces competition and co-evolution in relation to plant disease suppression. Res Microbiol 163:490–499

    Article  PubMed  Google Scholar 

  • Kourtev P, Ehrenfeld J, Häggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905

    Article  CAS  Google Scholar 

  • Kowalchuk G, Buma D, De Boer W, Klinkhamer P, Van Veen J (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Anton van Leeuw 81:509–520

    Article  Google Scholar 

  • Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci U S A 109:14058–14062

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lupwayi NZ, Rice WA, Clayton GW (1998) Soil microbial diversity and community structure under wheat as influenced by tillage and crop rotation. Soil Biol Biochem 30:1733–1741

    Article  CAS  Google Scholar 

  • Marilley L, Aragno M (1999) Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots. Appl Soil Ecol 13:127–136

    Article  Google Scholar 

  • Marschner P, Yang C-H, Lieberei R, Crowley D (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445

    Article  CAS  Google Scholar 

  • Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208

    Article  CAS  Google Scholar 

  • Mercik S (1994) The most important soil properties and yields in long-term static fertilization experiments at Skierniewice. Roczniki Gleboznawcze 44:71–78

    Google Scholar 

  • Nacke H, Thürmer A, Wolherr A, Will C, Hodac L et al (2011) Pyrosequencing-Based Assessment of Bacterial Community Structure Along Different Management Types in German Forest and Grassland Soils. PLoS One 6(2):e17000. doi:10.1371/journal.pone.0017000

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara RB (2005) Vegan: community ecology package Version 17–81 http://cran.r-projectorg/

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0, URL http://www.R-projectorg/

  • Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sattell R, Dick R, Karow R, Kaufman D, Hemphill D, Luna J, McGrath D (1998) Cereal Rye. Oregon State University Extension Service. http://ir.library.oregonstate.edu/xmlui/bitstream/handle/1957/14957/em8694.pdf. Accessed 20 May 2014

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Horn DJV, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shange RS, Ankumah RO, Ibekwe AM, Zabawa R, Dowd SE (2012) Distinct soil bacterial communities revealed under a diversely managed agroecosystem. PLoS One 7(7):e40338. doi:10.1371/journal.pone.0040338

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Steer J, Harris JA (2000) Shifts in the microbial community in rhizosphere and non-rhizosphere soils during the growth of Agrostis stolonifera. Soil Biol Biochem 32:869–878

    Article  CAS  Google Scholar 

  • Teixeira LCRS, Peixoto RS, Cury JC, Sul WJ, Pellizari VH, Tiedje J, Rosado AS (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J 4:989–1001

    Article  PubMed  Google Scholar 

  • Uroz S, Buée M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microb Rep 2:281–288

    Article  CAS  Google Scholar 

  • Uroz S, Oger P, Moring E, Frey-Klett P (2012) Distinct ectomycorrhizospheres share similar bacterial communities as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl Environ Microbiol 78:3020–3024

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van Der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Wiklander L (1974) The acidification of soil by acid precipitation. Grundforbaettring 26:155–164

    Google Scholar 

  • Yin C, Jones KL, Peterson DE, Garrett KA, Hulbert SH, Paulitz TC (2010) Members of soil bacterial communities sensitive to tillage and crop rotation. Soil Biol Biochem 42:2111–2118

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Ronald Faber at the Sand Plain Research Farm for assistance with soil selection and history. We also thank Chris Wright at the Roy Carver Biotechnology Center for assistance with sample preparation for pyrosequencing. Also thanks to Laura Felice, Jon Anderson and Phil Manlick for assistance with plant harvesting and processing. Thanks to Pat Schloss and Sarah Westcott for advice with sequence processing via Mothur and to the Minnesota Supercomputing Institute for use of computing resources. This research was funded by National Science Foundation Microbial Observatories Program (Grant #9,977,907), United States Department of Agriculture Microbial Observatories (Grant # 2006-35,319-17,445), USDA-NIFA (Grant # 2011 67,019-30,330), and the University of Minnesota Agricultural Experiment Station Project (#MIN 22–018).

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Authors and Affiliations

  1. Department of Plant Pathology, University of Minnesota, 495 Borlaug Hall 1991 Upper Buford Circle, Saint Paul, MN, 55108, USA

    B. E. Arenz, J. M. Bradeen, L. K. Otto-Hanson & L. L. Kinkel

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  1. B. E. Arenz
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  2. J. M. Bradeen
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  3. L. K. Otto-Hanson
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  4. L. L. Kinkel
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Correspondence to B. E. Arenz.

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Responsible Editor: Gera Hol.

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Arenz, B.E., Bradeen, J.M., Otto-Hanson, L.K. et al. Two grass species fail to display differing species-specific effects on soil bacterial community structures after one season of greenhouse growth. Plant Soil 385, 241–254 (2014). https://doi.org/10.1007/s11104-014-2226-2

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