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Bacterial Diversity in the Rhizosphere of Cucumbers Grown in Soils Covering a Wide Range of Cucumber Cropping Histories and Environmental Conditions

  • Plant Microbe Interactions
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Abstract

Rhizosphere microorganisms in soils are important for plant growth. However, the importance of rhizosphere microorganisms is still underestimated since many microorganisms associated with plant roots cannot be cultured and since the microbial diversity in the rhizosphere can be influenced by several factors, such as the cropping history, biogeography, and agricultural practice. Here, we characterized the rhizosphere bacterial diversity of cucumber plants grown in soils covering a wide range of cucumber cropping histories and environmental conditions by using pyrosequencing of bacterial 16S rRNA genes. We also tested the effects of compost addition and/or bacterial inoculation on the bacterial diversity in the rhizosphere. We identified an average of approximately 8,883 reads per sample, corresponding to around 4,993 molecular operational taxonomic units per sample. The Proteobacteria was the most abundant phylum in almost all soils. The abundances of the phyla Bacteroidetes, Actinobacteria, Firmicutes, Acidobacteria, and Verrucomicrobia varied among the samples, and together with Proteobacteria, these phyla were the six most abundant phyla in almost all analyzed samples. Analyzing all the sample libraries together, the predominant genera found were Flavobacterium, Ohtaekwangia, Opitutus, Gp6, Steroidobacter, and Acidovorax. Overall, compost and microbial amendments increased shoot biomass when compared to untreated soils. However, compost addition decreased the bacterial α-diversity in most soils (but for three soils compost increased diversity), and no statistical effect of microbial amendment on the bacterial α-diversity was found. Moreover, soil amendments did not significantly influence the bacterial β-diversity. Soil organic content appeared more important than compost and microbial amendments in shaping the structure of bacterial communities in the rhizosphere of cucumber.

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References

  1. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  CAS  PubMed  Google Scholar 

  2. Jackson LE, Bowles TM, Hodson AK, Lazcano C (2012) Soil microbial-root and microbial-rhizosphere processes to increase nitrogen availability and retention in agroecosystems. Curr Opin Environ Sustain 4:517–522

    Article  Google Scholar 

  3. Schenk PM, Carvalhais LC, Kazan K (2012) Unraveling plant–microbe interactions: can multi-species transcriptomics help? Trends Biotechnol 30:177–184

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  5. Newton AC, Fitt BD, Atkins SD, Walters DR, Daniell TJ (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends Microbiol 18:365–373

    Article  CAS  PubMed  Google Scholar 

  6. Teixeira LC, 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 

  7. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100

    Article  CAS  PubMed  Google Scholar 

  8. Buée M, De Boer W, Martin F, Van OL, Jurkevitch E (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321:189–212

    Article  Google Scholar 

  9. Mazurier S, Corberand T, Lemanceau P, Raaijmakers JM (2009) Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J 3:977–991

    Article  CAS  PubMed  Google Scholar 

  10. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F et al (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416

    Article  PubMed  Google Scholar 

  11. Morris RM, Nunn BL, Frazar C, Goodlett DR, Ting YS, Rocap G (2010) Comparative metaproteomics reveals ocean-scale shifts in microbial nutrient utilization and energy transduction. ISME J 4:673–685

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  13. Bressan M, Roncato MA, Bellvert F, Comte G, Haichar ZF, Achouak W, Berge O (2009) Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J 3:1243–1257

    Article  CAS  PubMed  Google Scholar 

  14. DeAngelis KM, Brodie EL, DeSantis TZ, Andersen GL, Lindow SE, Firestone MK (2008) Selective progressive response of soil microbial community to wild oat roots. ISME J 3:168–178

    Article  PubMed  Google Scholar 

  15. 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 

  16. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D et al (2013) Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. ISME J 7:2248–2258

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Bennett AJ, Bending GD, Chandler DC, Hilton S, Mills P (2012) Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations. Biol Rev 87:52–71

    Article  PubMed  Google Scholar 

  20. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351

    Article  PubMed  Google Scholar 

  21. Reeve JR, Schadt CW, Carpenter-Boggs L, Kang S, Zhou J, Reganold JP (2010) Effects of soil type and farm management on soil ecological functional genes and microbial activities. ISME J 4:1099–1107

    Article  PubMed  Google Scholar 

  22. Jesus ED, Marsh TL, Tiedje JM, Moreira FMD (2009) Changes in lands use alter the structure of bacterial communities in Western Amazon soils. ISME J 3:1004–1011

    Article  Google Scholar 

  23. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. 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 57:5111–5120

    Article  Google Scholar 

  25. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281

    Article  CAS  PubMed  Google Scholar 

  26. Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139

    Article  CAS  Google Scholar 

  27. Ye SF, Yu JQ, Peng YH, Zheng JH, Zou LY (2004) Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant Soil 263:143–150

    Article  CAS  Google Scholar 

  28. Zhou X, Wu F (2012) Effects of amendments of ferulic acid on soil microbial communities in the rhizosphere of cucumber (Cucumis sativus L.). Eur J Soil Biol 50:191–197

    Article  CAS  Google Scholar 

  29. Ibekwe AM, Poss JA, Grattan SR, Grieve CM, Suarez D (2010) Bacterial diversity in cucumber (Cucumis sativus) rhizosphere in response to salinity, soil pH, and boron. Soil Biol Biochem 42:567–575

    Article  CAS  Google Scholar 

  30. Zhou X, Wu F (2013) Artificially applied vanillic acid changed soil microbial communities in the rhizosphere of cucumber (Cucumis sativus L.). Can J Soil Sci 93:13–21

    Article  CAS  Google Scholar 

  31. Chung S, Kong H, Buyer JS, Lakshman DK, Lydon J, Kim S-D, Roberts DP (2008) Isolation and partial characterization of Bacillus subtilis ME488 for suppression of soilborne pathogens of cucumber and pepper. Appl Microbiol Biotechnol 280:115–123

    Article  Google Scholar 

  32. Ofek M, Hadar Y, Minz D (2011) Colonization of cucumber seeds by bacteria during germination. Environ Microbiol 13:2794–2807

    Article  PubMed  Google Scholar 

  33. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL, Hanski I, Marden JH (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol Ecol 17:1636–1647

    Article  CAS  PubMed  Google Scholar 

  34. Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:118–123

    Article  CAS  PubMed  Google Scholar 

  35. Kuczynski J, Lauber CL, Walters WA, Parfrey LW, Clemente JC, Gevers D, Knight R (2011) Experimental and analytical tools for studying the human microbiome. Nat Rev Genet 13:47–58

    Article  PubMed  Google Scholar 

  36. Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, Ochman H, Hugenholtz P (2010) Experimental factors affecting PCR based estimates of microbial species richness and evenness. ISME J 4:642–647

    Article  CAS  PubMed  Google Scholar 

  37. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Tian Y, Zhang X, Liu J, Gao L (2011) Effects of summer cover crop and residue management on cucumber growth in intensive Chinese production systems: soil nutrients, microbial properties and nematodes. Plant Soil 339:299–315

    Article  CAS  Google Scholar 

  39. Shanon CE, Weaver W (1949) The mathematical theory of communications. University of Illinois Press, Urbana

    Google Scholar 

  40. Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270

    Google Scholar 

  41. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al (2013) Package ‘Vegan’, Community Ecology Package. Version 2.0-8. http://cran.r-project.org. Accessed July 10, 2013

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  43. Mahaffee WF, Kloepper JW (1997) Temporal changes in the bacterial communities of soil, rhizosphere, and endorhiza associated with field-grown cucumber (Cucumis sativus L.). Microb Ecol 34:210–223

    Article  PubMed  Google Scholar 

  44. Zhou X, Wu F (2012) p-Coumaric ccid influenced cucumber rhizosphere soil microbial communities and the growth of Fusarium oxysporum f. sp. cucumerinum owen. PLoS One 7:e48288

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. Xu Y, Wang G, Jin J, Liu J, Zhang Q, Liu X (2009) Bacterial communities in soybean rhizosphere in response to soil type, soybean genotype, and their growth stage. Soil Biol Biochem 41:919–925

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  47. Gottel NR, Castro HF, Kerley M, Yang Z, Pelletier DA, Podar M et al (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl Environ Microbiol 77:5934–5944

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3:992–1000

    Article  CAS  PubMed  Google Scholar 

  49. Naumoff DG, Dedysh SN (2012) Lateral gene transfer between the Bacteroidetes and Acidobacteria: the case of α-L-Rhamnosidases. FEBS Lett 586:3843–3851

    Article  CAS  PubMed  Google Scholar 

  50. Leggett MJ, McDonnell G, Denyer SP, Setlow P, Maillard JY (2012) Bacterial spore structures and their protective role in biocide resistance. J Appl Microbiol 113:485–498

    Article  CAS  PubMed  Google Scholar 

  51. Qin S, Xing K, Jiang JH, Xu LH, Li WJ (2011) Biodiversity, bioactive natural products and biotechnological potential of plant-associated endophytic actinobacteria. Appl Microbiol Biotechnol 89:457–473

    Article  CAS  PubMed  Google Scholar 

  52. Kim JS, Dungan RS, Kwon SW, Weon HY (2006) The community composition of root-associated bacteria of the tomato plant. World J Microbiol Biotechnol 22:1267–1273

    Article  CAS  Google Scholar 

  53. Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60:157–166

    Article  PubMed  Google Scholar 

  54. Germida JJ, Siciliano SD, de Freitas JR, Seib AM (1998) Diversity of root-associated bacteria associated with held-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26:43–50

    Article  CAS  Google Scholar 

  55. Bernardet JF, Bowman JP (2006) The genus Flavobacterium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, vol 7, 3rd edn. Springer, New York, pp 481–531

    Chapter  Google Scholar 

  56. Tejeda-Agredano MC, Gallego S, Vila J, Grifoll M, Ortega-Calvo JJ, Cantos M (2013) Influence of the sunflower rhizosphere on the biodegradation of PAHs in soil. Soil Biol Biochem 57:830–840

    Article  CAS  Google Scholar 

  57. Zhang YZ, Wang ET, Li M, Li QQ, Zhang YM, Zhao SJ et al (2011) Effects of rhizobial inoculation, cropping systems and growth stages on endophytic bacterial community of soybean roots. Plant Soil 347:147–161

    Article  CAS  Google Scholar 

  58. Gaggìa F, Baffoni L, Di Gioia D, Accorsi M, Bosi S, Marotti I et al (2013) Inoculation with microorganisms of Lolium perenne L.: evaluation of plant growth parameters and endophytic colonization of roots. New Biotechnol 30:695–704

    Article  Google Scholar 

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Acknowledgments

We are grateful to the Chinese Universities Scientific Fund (2014JD047 and 2014XJ035) and Beijing Innovation Team for Fruity Vegetables in Chinese Modern Agricultural Technology System for their financial supports.

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Correspondence to Yongqiang Tian or Lihong Gao.

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Tian, Y., Gao, L. Bacterial Diversity in the Rhizosphere of Cucumbers Grown in Soils Covering a Wide Range of Cucumber Cropping Histories and Environmental Conditions. Microb Ecol 68, 794–806 (2014). https://doi.org/10.1007/s00248-014-0461-y

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