Skip to main content
SpringerLink
Log in

Soil microbial communities in cucumber monoculture and rotation systems and their feedback effects on cucumber seedling growth

Plant and Soil volume 415, pages 507–520 (2017)Cite this article

Abstract

Background and aims

Loss of biodiversity caused by intensive agriculture is a major worldwide concern. Crop rotation can enhance crop productivity and increase soil microbial diversity. However, the functional significances of changes in soil microbial communities are poorly understood.

Methods

Soil microbial communities from a cucumber monoculture system and the cucumber season of a two-year rotation system (tomato-celery-cucumber-Chinese cabbage) were analyzed by quantitative PCR and high throughput amplicon sequencing. Then, feedback effects of soil biota on cucumber seedlings were evaluated through soil sterilization, addition of soil inoculum, and application of bactericide and fungicide.

Results

Crop rotation increased cucumber yield and bacterial diversity, but decreased fungal diversity and abundance. The bacterial and fungal community compositions also differed between the two cropping systems. Abundances of potential plant pathogens and antagonistic microorganisms were lower while potential plant-growth-promoting microorganisms were higher in the rotation system. The overall effect of soil biota was positive on cucumber seedling growth, and was stronger in the rotation system.

Conclusions

Increasing temporal plant diversity can change soil microbial communities and enhance crop productivity through positive plant-soil feedbacks mediated by soil biota.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

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

Similar content being viewed by others

References

  • Almario J, Moenne-Loccoz Y, Muller D (2013) Monitoring of the relation between 2,4-diacetylphloroglucinol-producing Pseudomonas and Thielaviopsis basicola populations by real-time PCR in tobacco black root-rot suppressive and conducive soils. Soil Biol Biochem 57:144–155

    Article  CAS  Google Scholar 

  • Badri DV, Chaparro JM, Zhang R, Shen Q, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bainard LD, Koch AM, Gordon AM, Klironomos JN (2013) Growth response of crops to soil microbial communities from conventional monocropping and tree-based intercropping systems. Plant Soil 363:345–356

    Article  CAS  Google Scholar 

  • Bakker MG, Otto-Hanson L, Lange AJ, Bradeen JM, Kinkel LL (2013) Plant monocultures produce more antagonistic soil Streptomyces communities than high-diversity plant communities. Soil Biol Biochem 65:304–312

    Article  CAS  Google Scholar 

  • Bálint M, Bartha L, O’Hara RB, Olson MS, Otte J, Pfenninger M, Robertson A, Tiffin P, Schmitt I (2015) Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars. Mol Ecol 24:235–248

    Article  PubMed  Google Scholar 

  • Bashan Y, de-Bashan LE (2002) Reduction of bacterial speck (Pseudomonas syringae pv. tomato) of tomato by combined treatments of plant growth-promoting bacterium, Azospirillum brasilense, streptomycin sulfate, and chemo-thermal seed treatment. Eur J Plant Pathol 108:821–829

  • Belay A, Claassens AS, Wehner FC (2002) Effect of direct nitrogen and potassium and residual phosphorous fertilizers on soil chemical properties, microbial components and maize yield under long term crop rotation. Biol Fert Soils 35:420–427

    Article  CAS  Google Scholar 

  • Brakhage AA (2013) Regulation of fungal secondary metabolism. Nat Rev Microbiol 11:21–32

    Article  CAS  PubMed  Google Scholar 

  • Brinkman EP, Van der Putten WH, Bakker EJ, Verhoeven KJF (2010) Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073

    Article  Google Scholar 

  • Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004) Soil fungi alter interactions between the invader Centaurea maculosa and north American natives. Ecology 85:1062–1071

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67

    Article  CAS  PubMed  Google Scholar 

  • Cong WF, Hoffland E, Li L, Six J, Sun JH, Bao XG, Zhang FS, van der Werf W (2015) Intercropping enhances soil carbon and nitrogen. Glob Change Biol 21:1715–1726

    Article  Google Scholar 

  • Cook RJ (2006) Toward cropping systems that enhance productivity and sustainability. PNAS 103:18389–18394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crowther TW, Maynard DS, Leff JW, Oldfield EE, McCulley RL, Fierer N, Bradford MA (2014) Predicting the responsiveness of soil biodiversity to deforestation: a cross-biome study. Glob Chang Biol 20:2983–2994

    Article  PubMed  Google Scholar 

  • Dalton BR, Weed SB, Blum U (1987) Plant phenolic acids in soils: a comparison of extraction procedures. Soil Sci Soc Amer J 51:1515–1521

    Article  CAS  Google Scholar 

  • de Souza JT, Raaijmakers JM (2003) Polymorphisms within the prnD and pltC genes from pyrrolnitrin and pyoluteorin-producing Pseudomonas and Burkholderia spp. FEMS Microbiol Ecol 43:21–34

    Article  PubMed  Google Scholar 

  • Derakhshani H, Tun HM, Khafipour E (2016) An extended single-index multiplexed 16S rRNA sequencing for microbial community analysis on MiSeq illumina platforms. J Basic Microbiol 56:321–326

    Article  CAS  PubMed  Google Scholar 

  • DeRito CM, Madsen EL (2009) Stable isotope probing reveals Trichosporon yeast to be active in situ in soil phenol metabolism. ISME J 3:477–485

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  • Eisenhauer N, Bessler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais AC, Scherber C, Steinbeiss S, Weigelt A, Weisser WW, Scheu S (2010) Plant diversity effects on soil microorganisms support the singular hypothesis. Ecology 91:485–496

    Article  CAS  PubMed  Google Scholar 

  • Eisenhauer N, Milcu A, Sabais ACW, Bessler H, Brenner J, Engels C, Klarner B, Maraun M, Partsch S, Roscher C, Schonert F, Temperton VM, Thomisch K, Weigelt A, Weisser WW, Scheu S (2011) Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term. PLoS One 6:e16055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes AD, Redi JNS, Macklaim JM, McMurrough TA, Edgell DR, Gloor GB (2014) Unifying the analysis of high-throughput sequencing datasets: characterizing RNA-seq, 16S rRNA gene sequencing and selective growth experiments by compositional data analysis. Microbiome 2:15

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Garbeva P, van Veen JA, van Elsas JD (2004) Assessment of the diversity, and antagonism towards Rhizoctonia solani AG3, of Pseudomonas species in soil from different agricultural regimes. FEMS Microbiol Ecol 47:51–64

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhiza and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432

    Article  Google Scholar 

  • Hu P, Hollister EB, Somenahally AC, Hons FM, Gentry TJ (2015) Soil bacterial and fungal communities respond differently to various isothiocyanates added for biofumigation. Front Microbiol 5:729

    Article  PubMed  PubMed Central  Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiß M, Larsson KH (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  Google Scholar 

  • Latz E, Eisenhauer N, Rall BC, Allan E, Roscher C, Scheu S, Jousset A (2012) Plant diversity improves protection against soil-borne pathogens by fostering antagonistic bacterial communities. J Ecol 100:597–604

    Article  Google Scholar 

  • Latz E, Eisenhauer N, Scheu S, Jousset A (2015) Plant identity drives the expression of biocontrol factors in a rhizosphere bacterium across a plant diversity gradient. Funct Ecol 29:1225–1234

    Article  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  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748

    Article  CAS  PubMed  Google Scholar 

  • Maron JL, Marler M, Klironomos JN, Cleveland CC (2011) Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol Lett 14:36–41

    Article  PubMed  Google Scholar 

  • Matthiessen JN, Kirkegaard JA (2006) Biofumigation and enhanced biodegradation: opportunity and challenge in soilborne pest and disease management. Crit Rev Plant Sci 25:235–265

    Article  CAS  Google Scholar 

  • Mavrodi OV, Mavrodi DV, Parejko JA, Thomashow LS, Weller DM (2012) Irrigation differentially impacts populations of indigenous antibiotic-producing Pseudomonas spp. in the rhizosphere of wheat. Appl Environ Microbiol 78:3214–3220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 

  • McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531

    Article  PubMed  PubMed Central  Google Scholar 

  • Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes encoding for 16S rRNA. Appl Environ Microbiol 59:695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nijjer S, Rogers WE, Siemann E (2007) Negative plant–soil feedbacks may limit persistence of an invasive tree due to rapid accumulation of soil pathogens. Proc R Soc B 274:2621–2627

    Article  PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens MHH, Wagner H (2014) Package ‘vegan’. Community Ecology Package, R Package Version 2:2

    Google Scholar 

  • Qian P, Wolt JD (1990) Effects of drying and time of incubation on the composition of displaced soil solution. Soil Sci 149:367–374

    Article  CAS  Google Scholar 

  • Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Change Biol 18:1918–1927

    Article  Google Scholar 

  • Sanchez S, Guzmán-Trampe S, Ávalos M, Ruiz B, Rodríguez-Sanoja R, Jiménez-Estrada M (2012) Microbial natural products. In: Civjan N (ed) Natural products in chemical biology. Wiley, Inc, Hoboken, pp 65–108

    Chapter  Google Scholar 

  • Sanford RA, Wagner DD, Wu QZ, Chee-Sanford JC, Thomas SH, Cruz-Garcia C, Rodriguez G, Massol-Deya A, Krishnani KK, Ritalahti KM, Nissen S, Konstantinidis KT, Loffler FE (2012) Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. PNAS 109:19709–19714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scarlett K, Tesoriero L, Daniel R, Guest D (2013) Detection and quantification of Fusarium oxysporum f. Sp. cucumerinum in environmental samples using a specific quantitative PCR assay. Eur J Plant Pathol 137:315–324

    Article  CAS  Google Scholar 

  • Schlatter DC, Bakker MG, Bradeen JM, Kinkel LL (2015) Plant community richness and microbial interactions structure bacterial communities in soil. Ecology 96:134–142

    Article  PubMed  Google Scholar 

  • Schnitzer SA, Klironomos JN, HilleRisLambers J, Kinkel LL, Reich PB, Xiao K, Rillig MC, Sikes BA, Callaway RM, Mangan SA (2011) Soil microbes drive the classic plant diversity-productivity pattern. Ecology 92:296–303

    Article  PubMed  Google Scholar 

  • Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140:339–353

    Article  Google Scholar 

  • Tian HL, Zhao JY, Zhang HY, Chi CQ, Li BA, Wu XL (2015) Bacterial community shift along with the changes in operational conditions in a membrane-aerated biofilm reactor. Appl Microbiol Biotechnol 99:3279–3290

    Article  CAS  PubMed  Google Scholar 

  • Tiemann LK, Grandy AS, Atkinson EE, Marin-Spiotta E, McDaniel MD (2015) Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecol Lett 18:761–771

    Article  CAS  PubMed  Google Scholar 

  • van der Heijden MGA, Wagg C (2013) Soil microbial diversity and agro-ecosystem functioning. Plant Soil 363:1–5

    Article  CAS  Google Scholar 

  • van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde TFJ, Wardle DA (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276

    Article  Google Scholar 

  • Verbruggen E, Kiers ET, Bakelaar PNC, Roling WFM, van der Heijden MGA (2012) Provision of contrasting ecosystem services by soil communities from different agricultural fields. Plant Soil 350:43–55

    Article  CAS  Google Scholar 

  • Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. PNAS 111:5266–5270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886

    Article  PubMed  Google Scholar 

  • Wu F, Yu H, Yu G, Pan K, Bao J (2011) Improved bacterial community diversity and cucumber yields in a rotation with kidney bean-celery-cucumber. Acta Agr Scand Sect B-Soil Pl 61:122–128

    Google Scholar 

  • Zhou X, Wu F (2012) p-Coumaric acid influenced cucumber rhizosphere soil microbial communities and the growth of Fusarium oxysporum f. sp. cucumerinum Owen. PloS one 7:e48288

  • Zhou X, Yu G, Wu F (2011) Effects of intercropping cucumber with onion or garlic on soil enzyme activities, microbial communities and cucumber yield. Eur J Soil Biol 47:279–287

    Article  CAS  Google Scholar 

  • Zhou X, Yu G, Wu F (2012) Soil phenolics in a continuously mono-cropped cucumber (Cucumis sativus L.) system and their effects on cucumber seedling growth and soil microbial communities. Eur J Soil Sci 63:332–340

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (41401271), China Postdoctoral Science Foundation (2015 T80320), University Nursing Program for Young Scholars with Creative Talents in Heilongjiang Province (UNPYSCT-2015002), China Agricultural Research System (CARS-25-08) and ‘Young Talents’ Project of Northeast Agricultural University (14QC08).

Author information

Authors and Affiliations

  1. Department of Horticulture, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Xingang Zhou, Jie Liu & Fengzhi Wu

  2. Postdoctoral Station of Biology, Northeast Agricultural University, Harbin, 150030, People’s Republic of China

    Xingang Zhou

  3. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture, Harbin, 150030, People’s Republic of China

    Fengzhi Wu

Authors
  1. Xingang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fengzhi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fengzhi Wu.

Additional information

Responsible Editor: Jeff R. Powell.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, X., Liu, J. & Wu, F. Soil microbial communities in cucumber monoculture and rotation systems and their feedback effects on cucumber seedling growth. Plant Soil 415, 507–520 (2017). https://doi.org/10.1007/s11104-017-3181-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3181-5

Keywords

search

Navigation