Advertisement

Biology and Fertility of Soils

, Volume 55, Issue 2, pp 109–120 | Cite as

Long-term silicate fertilization increases the abundance of Actinobacterial population in paddy soils

  • Sandipan Samaddar
  • Jaak Truu
  • Poulami Chatterjee
  • Marika Truu
  • Kiyoon Kim
  • Sukjin Kim
  • Sundaram Seshadri
  • Tongmin SaEmail author
Original Paper
  • 432 Downloads

Abstract

Silicon (Si) is widely used in improving crop yield, but effect of its application on soil bacterial community composition is poorly known. Quantitative PCR and high-throughput sequencing targeting the bacterial 16S rRNA gene were employed to characterize the bacterial community composition of long-term fertilized paddy soils treated with nitrogen (N), phosphorus (P), potassium (K), and Si (NPK + Si), with NPK or not fertilized (control). The NPK + Si fertilization significantly increased the urease and dehydrogenase activity. The relative abundance of Actinobacteria was significantly higher in the NPK + Si soil than in other two soils. Linear discriminant analysis (LDA) and effect size (LEfSe) analysis demonstrated that Actinobacteria and its associated taxonomic groups were significantly more abundant in the NPK + Si-treated plots. The bacterial community composition of the NPK + Si soil was significantly different from those of NPK and control soils as shown by the ordination plot. According to distance-based regression analysis, variation in bacterial community composition was related to available SiO2 and P2O5 concentrations. Functional profiles predicted from 16S rRNA abundance data showed that the NPK + Si plots were more enriched by genes coding enzymes related to plant growth promotion compared to NPK and control plots.

Keywords

Paddy fields Long-term silicate fertilization Bacterial diversity Actinobacterial enrichment Functional analysis 

Notes

Funding information

The authors would like to thank the Basic Science Research Program of the National Research Foundation (NRF) under the Ministry of Education, Science, and Technology (2015R1A2A1A05001885), South Korea for providing funding support towards the completion of this study. This study was also partially supported by the Estonian Research Council (grant IUT2-16) and through the European Regional Development Fund through Centre of Excellence EcolChange.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

374_2018_1335_MOESM1_ESM.docx (253 kb)
ESM 1 (DOCX 253 kb)

References

  1. Ahn JH, Song J, Kim BY, Kim MS, Joa JH, Weon HY (2012) Characterization of the bacterial and archaeal communities in rice field soils subjected to long-term fertilization practices. J Microbiol 50:754–765.  https://doi.org/10.1007/s12275-012-2409-6 CrossRefGoogle Scholar
  2. Ahn JH, Lee SA, Kim JM, Kim MS, Song J, Weon HY (2016) Dynamics of bacterial communities in rice field soils as affected by different long-term fertilization practices. J Microbiol 54:724–731.  https://doi.org/10.1007/s12275-016-6463-3 CrossRefGoogle Scholar
  3. Aislabie J, Deslippe JR, Dymond JR (2013) Soil microbes and their contribution to soil services. In: Dymond JR (ed) Ecosyst services in New Zealand: conditions and trends. Manaaki Whenua Press, Lincoln, New Zealand, pp 143–161Google Scholar
  4. Anderson MJ (2004) DISTLM v. 5: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics. University of Auckland, New Zealand, p 10Google Scholar
  5. Anderson MJ, Gorley RN, Clarke RK (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New ZealandGoogle Scholar
  6. Asada R, Tazaki K (2001) Silica biomineralization of unicellular microbes under strongly acidic conditions. Can Mineral 39:1–16CrossRefGoogle Scholar
  7. Badr MA, Shafei AM, El-deen SHS (2006) The dissolution of K and P-bearing minerals by silicate dissolving bacteria and their effect on sorghum growth. Res J Agric Biol Sci 2:5–11Google Scholar
  8. 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.  https://doi.org/10.1007/s11104-012-1321-5 CrossRefGoogle Scholar
  9. Beauchamp EG, Trevors JT, Paul JW (1989) Carbon sources for bacterial denitrification. In: Stewart BA (ed) Advances in soil science. Springer, Berlin, pp 113–142CrossRefGoogle Scholar
  10. Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201.  https://doi.org/10.1016/j.jplph.2014.12.014 CrossRefGoogle Scholar
  11. Beyer L, Wachendorf C, Elsner D, Knabe R (1993) Suitability of dehydrogenase activity assay as an index of soil biological activity. Biol Fertil Soils 16:52–56.  https://doi.org/10.1007/BF00336515 CrossRefGoogle Scholar
  12. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350.  https://doi.org/10.1007/s11274-011-0979-9 CrossRefGoogle Scholar
  13. Bowler C, Van Camp W, Van Montagu M, Inzé D, Asada K (1994) Superoxide dismutase in plants. Crit Rev Plant Sci 13:199–218CrossRefGoogle Scholar
  14. Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agric Sci 55:11–33CrossRefGoogle Scholar
  15. Chatterjee P, Samaddar S, Anandham R, Kang Y, Kim K, Selvakumar G, Sa T (2017) Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth. Front Plant Sci 8:705.  https://doi.org/10.3389/fpls.2017.00705 CrossRefGoogle Scholar
  16. Conn VM, Walker AR, Franco CMM (2008) Endophytic Actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant-Microbe Interact 21:208–218CrossRefGoogle Scholar
  17. Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  18. Dai Z, Su W, Chen H, Barberán A, Zhao H, Yu M, Yu L, Brookes PC, Schadt CW, Chang SX, Xu J (2018) Long-term nitrogen fertilization decreases bacterial diversity and favors the growth of Actinobacteria and Proteobacteria in agro-ecosystems across the globe. Glob Chang Biol 24:3452–3461.  https://doi.org/10.1111/gcb.14163 CrossRefGoogle Scholar
  19. Daquiado AR, Kuppusamy S, Kim SY, Kim JH, Yoon YE, Kim PJ, Oh SH, Kwak YS, Lee YB (2016) Pyrosequencing analysis of bacterial community diversity in long-term fertilized paddy field soil. Appl Soil Ecol 108:84–91.  https://doi.org/10.1016/j.apsoil.2016.08.006 CrossRefGoogle Scholar
  20. Dong WY, Zhang XY, Dai XQ, Fu XL, Yang FT, Liu XY, Sun XM, Wen XF, Schaeffer S (2014) Changes in soil microbial community composition in response to fertilization of paddy soils in subtropical China. Appl Soil Ecol 84:140–147.  https://doi.org/10.1016/j.apsoil.2014.06.007 CrossRefGoogle Scholar
  21. Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 9:167–172CrossRefGoogle Scholar
  22. Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606.  https://doi.org/10.1016/0038-0717(88)90141-1 CrossRefGoogle Scholar
  23. Epstein E (1994) The anomaly of silicon in plant biology. Proc Natl Acad Sci 91:11–17.  https://doi.org/10.1073/pnas.91.1.11 CrossRefGoogle Scholar
  24. Feng Y, Yu Y, Tang H, Zu Q, Zhu J, Lin X (2015) The contrasting responses of soil microorganisms in two rice cultivars to elevated ground-level ozone. Environ Pollut 197:195–202.  https://doi.org/10.1016/j.envpol.2014.11.032 CrossRefGoogle Scholar
  25. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176.  https://doi.org/10.1016/S0038-0717(02)00251-1 CrossRefGoogle Scholar
  26. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci 103:626–631.  https://doi.org/10.1073/pnas.0507535103 CrossRefGoogle Scholar
  27. Fu X, Long Z, Wei S, Huang W (2009) Study of the effect of silicate bacterium fertilizer on rice soil microbe and fertility. Soil Fertil Sci China 5(17)Google Scholar
  28. Giagnoni L, Pastorelli R, Mocali S, Arenella M, Nannipieri P, Renella G (2016) Availability of different nitrogen forms changes the microbial communities and enzyme activities in the rhizosphere of maize lines with different nitrogen use efficiency. Appl Soil Ecol 98:30–38.  https://doi.org/10.1016/j.apsoil.2015.09.004 CrossRefGoogle Scholar
  29. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39.  https://doi.org/10.1016/j.micres.2013.09.009 CrossRefGoogle Scholar
  30. Gu HH, Qiu H, Tian T, Zhan SS, Deng THB, Chaney RL, Wang SZ, Tang YT, Morel JL, Qiu RL (2011) Mitigation effects of silicon rich amendments on heavy metal accumulation in rice (Oryza sativa L.) planted on multi-metal contaminated acidic soil. Chemosphere 83:1234–1240.  https://doi.org/10.1016/j.chemosphere.2011.03.014 CrossRefGoogle Scholar
  31. Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring,M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. doi:  https://doi.org/10.1128/MMBR.00050-14
  32. He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374.  https://doi.org/10.1111/j.1462-2920.2007.01358.x CrossRefGoogle Scholar
  33. Heczko J, Gselman A, Turinek M, Bavec M, Kristl J (2011) Organic carbon content in soils of long-term field trial: comparison of analytical methods. Agric 8:17–22Google Scholar
  34. Holmalahti J, Wright AV, Raatikainen O (1994) Variations in the spectra of biological activities of actinomycetes isolated from different soils. Lett Appl Microbiol 18:144–146CrossRefGoogle Scholar
  35. Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255.  https://doi.org/10.1371/journal.pgen.1000255 CrossRefGoogle Scholar
  36. Jenkins SN, Waite IS, Blackburn A, Husband R, Rushton SP, Manning DC, O’Donnell AG (2009) Actinobacterial community dynamics in long term managed grasslands. Antonie Van Leeuwenhoek 95:319–334.  https://doi.org/10.1007/s10482-009-9317-8 CrossRefGoogle Scholar
  37. Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72CrossRefGoogle Scholar
  38. Kavamura VN, Santos SN, da Silva JL, Parma MM, Ávila LA, Visconti A, Zucchi TD, Taketani RG, Andreote FD, de Melo IS (2013) Screening of Brazilian cacti rhizobacteria for plant growth promotion under drought. Microbiol Res 168:183–191.  https://doi.org/10.1016/j.micres.2012.12.002 CrossRefGoogle Scholar
  39. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821.  https://doi.org/10.1038/nbt.2676 CrossRefGoogle Scholar
  40. Lauwers AM, Heinen W (1974) Bio-degradation and utilization of silica and quartz. Arch Microbiol 95:67–78.  https://doi.org/10.1007/BF02451749 CrossRefGoogle Scholar
  41. Lee YB, Ha HS, Park BK, Cho JS, Kim PJ (2002) Effect of a fly ash and gypsum mixture on rice cultivation. Soil Sci Plant Nutr 48:171–178.  https://doi.org/10.1080/00380768.2002.10409188 CrossRefGoogle Scholar
  42. Lindsay WL (1979) Chemical equilibria in soils. John Wiley & Sons, New YorkGoogle Scholar
  43. Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R (2007) Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res 35:e120.  https://doi.org/10.1093/nar/gkm541 CrossRefGoogle Scholar
  44. Luo X, Fu X, Yang Y, Cai P, Peng S, Chen W, Huang Q (2016) Microbial communities play important roles in modulating paddy soil fertility. Sci Rep 6:1–12.  https://doi.org/10.1038/srep20326 CrossRefGoogle Scholar
  45. Ma JF, Takahashi E (1990) Effect of silicon on the growth and phosphprus uptake of rice. Plant Soil 126:115–119.  https://doi.org/10.1007/BF00041376 CrossRefGoogle Scholar
  46. Ma JF, Takahashi E (2002) Soil, fertilizer, and plant silicon research in Japan. ElsevierGoogle Scholar
  47. Ma JF (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Sci Plant Nutr 50:11–18.  https://doi.org/10.1080/00380768.2004.10408447 CrossRefGoogle Scholar
  48. Makabe S, Kakuda KI, Sasaki Y, Ando T, Fujii H, Ando H (2009) Relationship between mineral composition or soil texture and available silicon in alluvial paddy soils on the Shounai Plain, Japan. Soil Sci Plant Nutr 55:300–308.  https://doi.org/10.1111/j.1747-0765.2008.00352.x CrossRefGoogle Scholar
  49. Marques APGC, Pires C, Moreira H, Rangel AOSS, Castro PML (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235.  https://doi.org/10.1016/j.soilbio.2010.04.014 CrossRefGoogle Scholar
  50. Mcginnity P (2015) Silicon and its role in crop production. PhD thesis. http://planttuff.com/wp-content/uploads/2015/12/silicon-agriculture-iiterature-rvw-1.pdf
  51. Mingma R, Pathom-aree W, Trakulnaleamsai S, Thamchaipenet A, Duangmal K (2014) Isolation of rhizospheric and roots endophytic actinomycetes from Leguminosae plant and their activities to inhibit soybean pathogen, Xanthomonas campestris pv. glycine. World J Microbiol Biotechnol 30:271–280.  https://doi.org/10.1007/s11274-013-1451-9 CrossRefGoogle Scholar
  52. Nacke H, Thürmer A, Wollherr A, Will C, Hodac L, Herold N, Schöning I, Schrumpf M, Daniel R (2011) Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS One 6:e17000.  https://doi.org/10.1371/journal.pone.0017000 CrossRefGoogle Scholar
  53. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK, Obreson A, Frossard E (eds) Phosphorus in action. Springer, Berlin, pp 215–243CrossRefGoogle Scholar
  54. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19.  https://doi.org/10.1007/s00374-017-1245-6 CrossRefGoogle Scholar
  55. Nõlvak H, Truu M, Truu J (2012) Evaluation of quantitative real-time PCR workflow modifications on 16S rRNA and tetA gene quantification in environmental samples. Sci Total Environ 426:351–358.  https://doi.org/10.1016/j.scitotenv.2012.03.054 CrossRefGoogle Scholar
  56. Park W, Kim KS, Lee JE, Cha YL, Moon YH, Song YS, Jeong EG, Ahn SJ, Hong SW, Lee YH (2017) Effect of different application levels of rapeseed meal on growth and yield components of rice. Appl Biol Chem 60:403–410.  https://doi.org/10.1007/s13765-017-0291-y CrossRefGoogle Scholar
  57. Passari AK, Mishra VK, Singh G, Singh P, Kumar B, Gupta VK, Sharma RK, Saikia R, Donovan AO, Singh BP (2017) Insights into the functionality of endophytic Actinobacteria with a focus on their biosynthetic potential and secondary metabolites production. Sci Rep 7:1–17.  https://doi.org/10.1038/s41598-017-12235-4 CrossRefGoogle Scholar
  58. Peng QA, Shaaban M, Wu Y, Hu R, Wang B, Wang J (2016) The diversity of iron reducing bacteria communities in subtropical paddy soils of China. Appl Soil Ecol 101:20–27.  https://doi.org/10.1016/j.apsoil.2016.01.012 CrossRefGoogle Scholar
  59. Pham VHT, Kim J (2012) Cultivation of unculturable soil bacteria. Trends Biotechnol 30:475–484.  https://doi.org/10.1016/j.tibtech.2012.05.007 CrossRefGoogle Scholar
  60. Pollmann S, Neu D, Weiler EW (2003) Molecular cloning and characterization of an amidase from Arabidopsis thaliana capable of converting indole-3-acetamide into the plant growth hormone, indole-3-acetic acid. Phytochemistry 62:293–300.  https://doi.org/10.1016/S0031-9422(02)00563-0 CrossRefGoogle Scholar
  61. Ramirez KS, Lauber CL, Knight R, Bradford MA, Fierer N (2010) Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology 91:3463–3470.  https://doi.org/10.1890/10-0426.1 CrossRefGoogle Scholar
  62. Rangaraj S, Gopalu K, Rathinam Y, Periasamy P, Venkatachalam R, Narayanasamy K (2014) Effect of silica nanoparticles on microbial biomass and silica availability in maize rhizosphere. Biotechnol Appl Biochem 61:668–675.  https://doi.org/10.1002/bab.1191 CrossRefGoogle Scholar
  63. Rong Y, Wang Y, Guan Y, Ma J, Cai Z, Yang G, Zhao X (2017) Pyrosequencing reveals soil enzyme activities and bacterial communities impacted by graphene and its oxides. J Agric Food Chem 65:9191–9199.  https://doi.org/10.1021/acs.jafc.7b03646 CrossRefGoogle Scholar
  64. Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:. doi:  https://doi.org/10.1093/nar/gkp045
  65. Santoyo G, Moreno-Hagelsieb G, del Carmen O-MM, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99.  https://doi.org/10.1016/j.micres.2015.11.008 CrossRefGoogle Scholar
  66. 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, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.  https://doi.org/10.1128/AEM.01541-09 CrossRefGoogle Scholar
  67. Schloter M, Nannipieri P, Sørensen SJ, Elsas JDV (2018) Microbial indicators for soil quality. Biol Fertil Soils 54:1–10.  https://doi.org/10.1007/s00374-017-1248-3 CrossRefGoogle Scholar
  68. Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489.  https://doi.org/10.1007/s00374-017-1205-1 CrossRefGoogle Scholar
  69. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60.  https://doi.org/10.1186/gb-2011-12-6-r60 CrossRefGoogle Scholar
  70. Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M, Hurek T, Sarkar A, Bodrossy L, van Overbeek L, Brar D, van Elsas JD, Reinhold-Hurek B (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36.  https://doi.org/10.1094/MPMI-08-11-0204 CrossRefGoogle Scholar
  71. Shelobolina E, Roden E, Benzine J, Xiong MY (2014) Using phyllosilicate-Fe (II)-oxidizing soil bacteria to improve Fe and K plant nutrition. United States Patent Application US 14(/209):509Google Scholar
  72. Sugiyama A, Bakker MG, Badri DV, Manter DK, Vivanco JM (2013) Relationships between Arabidopsis genotype-specific biomass accumulation and associated soil microbial communities. Botany 91:123–126.  https://doi.org/10.1139/cjb-2012-0217 CrossRefGoogle Scholar
  73. Thalmann A (1968) Zur methodik der bestimmung der dehydrogenaseaktivitat im boden mittels triphenytetrazoliumchlorid (TTC). Landwirtsch Forsch 21:249–258Google Scholar
  74. Tubaña BS, Heckman JR (2015) Silicon in soils and plants. In: Rodrigues FA, Datnoff LE (eds) Silicon and plant diseases. Springer, Berlin, pp 7–51CrossRefGoogle Scholar
  75. Vaijayanthi G, Vijayakumar R, Dhanasekaran D (2016) Actinobacteria—a biofactory of novel enzymes. In: Dhanasekaran D, Jiang Y (eds) Actinobacteria-basics and biotechnological applications. InTechOpen, London, pp 329–352Google Scholar
  76. Van Oosten MJ, Pepe O, De Pascale S, Silletti S, Maggio A (2017) The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem Biol Technol Agric 4:1–12. doi:  https://doi.org/10.1186/s40538-017-0089-5
  77. Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484.  https://doi.org/10.1007/s00374-017-1191-3 CrossRefGoogle Scholar
  78. Walitang DI, Kim K, Madhaiyan M, Kim YK, Kang Y, Sa T (2017) Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of rice. BMC Microbiol 17:1–13.  https://doi.org/10.1186/s12866-017-1117-0 CrossRefGoogle Scholar
  79. Walitang DI, Kim CG, Kim K, Kang Y, Kim YK, Sa T (2018) The influence of host genotype and salt stress on the seed endophytic community of salt-sensitive and salt-tolerant rice cultivars. BMC Plant Biol 18:1–16.  https://doi.org/10.1186/s12870-018-1261-1 CrossRefGoogle Scholar
  80. Wang L, Cai K, Chen Y, Wang G (2013) Silicon-mediated tomato resistance against Ralstonia solanacearum is associated with modification of soil microbial community structure and activity. Biol Trace Elem Res 152:275–283.  https://doi.org/10.1007/s12011-013-9611-1 CrossRefGoogle Scholar
  81. Wang Y, Naumann U, Wright ST, Warton DI (2012) mvabund—an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474.  https://doi.org/10.1111/j.2041-210X.2012.00190.x CrossRefGoogle Scholar
  82. Wolińska A, Stępniewska Z (2012) Dehydrogenase activity in the soil environment. In: Canuto RA (ed) Dehydrogenases. InTechOpen, London, pp 183–210Google Scholar
  83. Wood SA, Gilbert JA, Leff JW, Fierer N, D’Angelo H, Bateman C, Gedallovich SM, Gillikin CM, Gradoville MR, Mansor P, Massmann A, Yang N, Turner BL, Brearley FQ, McGuire KL (2017) Consequences of tropical forest conversion to oil palm on soil bacterial community and network structure. Soil Biol Biochem 112:258–268.  https://doi.org/10.1016/j.soilbio.2017.05.019 CrossRefGoogle Scholar
  84. Xuan DT, Guong VT, Rosling A, Alström S, Chai B, Högberg N (2012) Different crop rotation systems as drivers of change in soil bacterial community structure and yield of rice, Oryza sativa. Biol Fertil Soils 48:217–225.  https://doi.org/10.1007/s00374-011-0618-5 CrossRefGoogle Scholar
  85. Yang M, Yang D, Yu X (2018) Soil microbial communities and enzyme activities in sea-buckthorn (Hippophae rhamnoides) plantation at different ages. PLoS One 13:1–15.  https://doi.org/10.1371/journal.pone.0190959 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Environmental and Biological ChemistryChungbuk National UniversityCheongjuRepublic of Korea
  2. 2.Faculty of Science and TechnologyUniversity of TartuTartuEstonia
  3. 3.Crop Cultivation and Environment Research DivisionNational Institute of Crop ScienceSuwonRepublic of Korea
  4. 4.Indigenous and Frontier Technology Research Centre (IFTR)ChennaiIndia

Personalised recommendations