Skip to main content

Advertisement

SpringerLink
Log in

Bacterial diversity in the rhizosphere of two phylogenetically closely related plant species across environmental gradients

  • Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Rhizosphere soil bacterial communities are crucial to plant growth, health, and stress resistance. In order to detect how bacterial communities associated with the rhizosphere of phylogenetically related plant species vary in terms of composition, function, and diversity, we investigated the rhizosphere bacterial community structure of two perennial shrub species, Caragana jubata and Caragana roborovskyi, under natural field conditions in northwest China and analyzed the influence of soil properties and environmental factors.

Materials and methods

Eighteen root samples, eight for C. jubata, and ten for C. roborovskyi, along with any adherent soil particles, were collected from multiple sites in northwest China. The rhizosphere soil was washed from the roots, and bacterial communities were analyzed using Illumina MiSeq sequencing of 16S rRNA gene amplicons. Then, α-diversity and β-diversity were calculated using QIIME.

Results and discussion

Across species, Proteobacteria (29 %), Actinobacteria (15 %), Chloroflexi (10 %), Acidobacteria (10 %), Bacteroidetes (8 %), Firmicutes (8 %), Planctomycetes (7 %), Gemmatimonadetes (4 %), and Verrucomicrobia (3 %) were the most abundant phyla in the rhizosphere of C. jubata and C. roborovskyi. However, principal co-ordinates analysis indicated strong interspecific patterns of bacterial rhizosphere communities. Further, the richness of Proteobacteria, Acidobacteria, Bacteroidetes, Verrucomicrobia, Firmicutes, and Nitrospirae was significantly higher in the rhizosphere of C. jubata compared with C. roborovskyi, while the opposite was found for Actinobacteria and Cyanobacteria. However, the Shannon index showed no significant difference in α-diversity between C. jubata and C. roborovskyi. Distance-based redundancy analysis indicated that soil properties and environmental factors exerted strong influences on the structure of the rhizosphere bacterial community and explained 47 and 46 % of community variances between samples, respectively.

Conclusions

Our results showed strong interspecific clustering of the bacterial rhizosphere communities of C. roborovskyi and C. jubata. Altitude explained most of the variation in the composition of bacterial rhizosphere communities of C. roborovskyi and C. jubata, followed by soil pH, water content, organic matter content, total nitrogen content, and mean annual rainfall.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andrew DR, Fitak RR, Munguia-Vega A, Racolta A, Martinson VG, Dontsova K (2012) Abiotic factors shape microbial diversity in Sonoran Desert soils. Appl Environ Microbiol 78(2):7527–7537

    Article  CAS  Google Scholar 

  • Aira M, Gómez-Brandón M, Lazcano C, Bååth E, Domínguez J (2010) Plant genotype strongly modifies the structure and growth of maize rhizosphere microbial communities. Soil Biol Biochem 42(12):2276–2281

    Article  CAS  Google Scholar 

  • Badri DV, Weir TL, Van Der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotech 20(6):642–650

    Article  CAS  Google Scholar 

  • Bais HP, Broeckling CD, Vivanco JM (2008) Root exudates modulate plant microbe interactions in the rhizosphere. In: Karlovsky P (ed) Secondary metabolites in soil ecology, soil biology 14. Springer, Berlin, Heidelberg, pp 241–252

    Chapter  Google Scholar 

  • Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8(2):217–230

    Article  Google Scholar 

  • Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486

    Article  CAS  Google Scholar 

  • Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fact 13:66–76

    Article  Google Scholar 

  • Broughton WJ, Zhang F, Perret X, Staehelin C (2003) Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives. Plant Soil 252(1):129–137

    Article  CAS  Google Scholar 

  • Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. The ISME journal 8:790–803

    Article  CAS  Google Scholar 

  • Chen Z, Wu W, Shao X, Li L, Guo Y, Ding G (2015) Shifts in abundance and diversity of soil ammonia-oxidizing bacteria and archaea associated with land restoration in a semi-arid ecosystem. PLoS One 10:e0132879

  • Chen XR, Li YP, Li QY, Xing YP, Liu BB, Tong YH, Xu JY (2016) SCR96, a small cysteine-rich secretory protein of Phytophthora cactorum, can trigger cell death in the Solanaceae and is important for the pathogenicity and oxidative stress tolerance. Mol Plant Pathol 17(4):577–87

  • de Groot A, Dulermo R, Ortet P, Blanchard L, Guérin P, Fernandez B, Vacherie B, Dossat C, Jolivet E, Siguier P, Chandler M, Barakat M, Dedieu A, Barbe V, Heulin T, Sommer S, Achouak W, Armengaud J (2009) Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet 5(3):e1000434

    Article  Google Scholar 

  • de Vrieze J (2015) The littlest farmhands. Science 349(6249):680–683

    Article  Google Scholar 

  • Fierer N, Ladau J, Clemente JC, Leff JW, Owens SM, Pollard KS, Knight R, Gilbert JA, McCulley RL (2013) Reconstructing the microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342(6158):621–624

    Article  CAS  Google Scholar 

  • Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso JG (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. Proc Natl Acad Sci U S A 109(52):21390–21395

    Article  CAS  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364

    Article  Google Scholar 

  • Fuerst JA (1995) The planctomycetes: emerging models for microbial ecology, evolution and cell biology. Microbiol 141(7):1493–1506

    Article  CAS  Google Scholar 

  • Gao LF, Hu ZA, Wang HX (2002) Genetic diversity of rhizobia isolated from Caragana intermedia in Maowusu sandland, north of China. Lett Appl Microbiol 35(4):347–352

    Article  CAS  Google Scholar 

  • Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13(6):1642–1654

    Article  Google Scholar 

  • Hannula SE, de Boer W, van Veen J (2012) A 3-year study reveals that plant growth stage, season and field site affect soil fungal communities while cultivar and GM-trait have minor effects. PLoS One 7(4):e33819

    Article  CAS  Google Scholar 

  • Hou X, Liu JE, Zhao YZ, Zhao LQ (2006) Interspecific relationships of Caragana microphylla, C. davazamcii and C. korshinskii (Leguminosae) based on ITS and trnL-F data sets. Acta Phytotaxon Sin 44:126–134

    Article  Google Scholar 

  • Innes L, Hobbs PJ, Bardgett RD (2004) The impacts of individual plant species on rhizosphere microbial communities in soils of different fertility. Biol Fertil Soils 40(1):7–13

    Article  Google Scholar 

  • Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72(3):1719–1728

    Article  CAS  Google Scholar 

  • Ji Z, Yan H, Cui Q, Wang E, Chen W, Chen W (2015) Genetic divergence and gene flow among Mesorhizobium strains nodulating the shrub legume Caragana. Syst Appl Microbiol 38(3):176–183

    Article  CAS  Google Scholar 

  • Khare E, Arora NK (2010) Effect of indole-3-acetic acid (IAA) produced by Pseudomonas aeruginosa in suppression of charcoal rot disease of chickpea. Curr Microbiol 61(1):64–68

    Article  CAS  Google Scholar 

  • Kowalchuk GA, Hol WHG, Van Veen JA (2006) Rhizosphere fungal communities are influenced by Senecio jacobaea pyrrolizidine alkaloid content and composition. Soil Biol Biochem 38(9):2852–2859

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lu YL, Chen WF, Wang ET, Guan SH, Yan XR, Chen WX (2009) Genetic diversity and biogeography of rhizobia associated with Caragana species in three ecological regions of China. Syst Appl Microbiol 32(5):351–361

    Article  CAS  Google Scholar 

  • Ma CC, Gao YB, Guo HY, Wang JL, Wu JB, Xu JS (2008) Physiological adaptations of four dominant Caragana species in the desert region of the Inner Mongolia Plateau. J Arid Environ 72(3):247–254

    Article  Google Scholar 

  • Madden NM, Southard RJ, Mitchell JP (2009) Soil water content and soil disaggregation by disking affects PM10 emissions. J Environ Qual 38:36–43

    Article  CAS  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963

    Article  Google Scholar 

  • Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Øvreås L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112

    Article  CAS  Google Scholar 

  • McLean EO (1982) Soil pH and lime requirement. In: Page AL (ed) Methods of soil analysis, part 2. American Soc. Agronomy, Madison, pp 199–224

    Google Scholar 

  • Meng QX, Niu Y, Niu XW, Roubin RH, Hanrahan JR (2009) Ethnobotany, phytochemistry and pharmacology of the genus Caragana used in traditional Chinese medicine. J Ethnopharmacol 124(3):350–368

    Article  CAS  Google Scholar 

  • Micallef SA, Shiaris MP, Colon-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J Exp Bot 60(6):1729–1742

    Article  CAS  Google Scholar 

  • Mougel C, Offre P, Ranjard L, Corberand T, Gamalero E, Robin C, Lemanceau P (2006) Dynamic of the genetic structure of bacterial and fungal communities at different developmental stages of Medicago truncatula Gaertn. cv. Jemalong line J5. New Phytol 170(1):165–175

    Article  CAS  Google Scholar 

  • Niu XF, Li YM, Hu H, Liu X, Qi L (2013) Chemical constituents from Caragana tangutica. Biochem Syst Ecol 51:288–290

    Article  CAS  Google Scholar 

  • Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A 110(16):6548–6553

    Article  CAS  Google Scholar 

  • Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182(2):314–330

    Article  CAS  Google Scholar 

  • Shakya M, Quince C, Campbell JH, Yang ZK, Schadt CW, Podar M (2013) Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities. Environ Microbiol 15(6):1882–1899

    Article  CAS  Google Scholar 

  • Shen CC, Xiong JB, Zhang HY, Feng YZ, Lin XG, Li XY, Liang WJ, Chu HY (2013) Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57:204–211

    Article  CAS  Google Scholar 

  • Sinha RK, Valani D, Chauhan K, Agarwal S (2010) Embarking on a second green revolution for sustainable agriculture by vermiculture biotechnology using earthworms: reviving the dreams of Sir Charles Darwin. J Agr Biot Sust Dev 2(7):113–128

    CAS  Google Scholar 

  • Siqueira GM, Dafonte JD, Armesto MV, França e Silva EF (2013) Using multivariate geostatistics to assess patterns of spatial dependence of apparent soil electrical conductivity and selected soil properties. Sci World J 2014:712403–712403

  • Šmilauer P, Lepš J (2014) Multivariate analysis of ecological data using CANOCO 5. Cambridge University Press

  • Spence CA, Raman V, Donofrio NM, Bais HP (2014) Global gene expression in rice blast pathogen Magnaporthe oryzae treated with a natural rice soil isolate. Planta 239(1):171–85

    Article  CAS  Google Scholar 

  • Tedersoo L, Bahram M, Põlme S et al (2014) Fungal biogeography. Global diversity and geography of soil fungi. Science 346(6213):1256688

    Article  Google Scholar 

  • Teixeira L, 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  Google Scholar 

  • Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14(6):209

    Article  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 Microbiol Rep 2(2):281–288

    Article  CAS  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267

    Article  CAS  Google Scholar 

  • Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006) White lupin has developed a complex strategy to limit microbial degradation of secreted citrate required for phosphate acquisition. Plant Cell Environ 29(5):919–927

    Article  CAS  Google Scholar 

  • Yan XR, Chen WF, Fu JF, Lu YL, Xue CY, Sui XH, Li Y, Wang ET, Chen WX (2007) Mesorhizobium spp. are the main microsymbionts of Caragana spp. grown in Liaoning Province of China. FEMS Microbiol Lett 271:265–273

    Article  CAS  Google Scholar 

  • Yuan YL, Si GC, Wang J, Luo TX, Zhang GX (2014) Bacterial community in alpine grasslands along an altitudinal gradient on the Tibetan Plateau. FEMS Microbiol Ecol 87:121–132

    Article  CAS  Google Scholar 

  • Zhang ML, Landiges YP, Nelson GS (2002) TASS and an analysis of the genus Caragana. Acta Bot Sin 44:1213–1218

    Google Scholar 

  • Zhang ML, Fritsch PW, Cruz BC (2009) Phylogeny of Caragana (Fabaceae) based on DNA sequence data from rbcL, trnS–trnG, and ITS. Mol Phylogenet Evol 50(3):547–559

    Article  CAS  Google Scholar 

  • Zhao YZ (2009) Classification and its floristic geography of Caragana Fabr. in the word. China. Inner Mongolia University Press, Inner Mongolia, China

Download references

Acknowledgments

This study was supported by grants from the National Natural Science Foundation of China (Nos. 31260166, 31360185, and 31560345).

Author information

Author notes

    Authors and Affiliations

    1. School of Life Science, Ningxia University, Yinchuan, 750021, People’s Republic of China

      Xiaofan Na & Ting Ting Xu

    2. Institute of Environmental Engineer, Ningxia University, Yinchuan, 750021, People’s Republic of China

      Ming Li & Fei Ma

    3. Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, 901 83, Umeå, Sweden

      Paul Kardol

    Authors
    1. Xiaofan Na
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Ting Ting Xu
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Ming Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Fei Ma
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Paul Kardol
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Fei Ma.

    Additional information

    Responsible editor: Chengrong Chen

    Xiaofan Na and Ting Ting Xu contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    ESM 1

    (DOCX 1440 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Na, X., Xu, T.T., Li, M. et al. Bacterial diversity in the rhizosphere of two phylogenetically closely related plant species across environmental gradients. J Soils Sediments 17, 122–132 (2017). https://doi.org/10.1007/s11368-016-1486-2

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11368-016-1486-2

    Keywords

    Search

    Navigation