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Impact of soil leachate on microbial biomass and diversity affected by plant diversity

  • Chao Zhang
  • Jie Wang
  • Guobin Liu
  • Zilin Song
  • Linchuan FangEmail author
Regular Article

Abstract

Aims

High plant diversity is usually linked with high soil microbial diversity, which is hypothesized to be attributed to a high diversity of components in the soil leachate, but experimental evidence is scarce. The aim of this study was to determine if the variation in soil leachate caused by plant diversity could affect the soil microbial community.

Methods

A microcosm experiment was conducted to determine the effect of plant diversity on the soil microbial community by measuring soil leachate in a gradient of plant richness from levels 1 (one species) to 3 (three species).

Results

Plant richness significantly affected the diversity of soil leachate and microbial communities. The amount and diversity of soil leachate, microbial biomass carbon (C), basal respiration, β-1,4-glucosidase activity, β-1,4-N-acetylglucosaminidase activity, bacterial biomass, fungal biomass, total microorganism biomass, and microbial diversity (Shannon diversity index and evenness) were highest at richness level 3. Changes in the microbial community were best explained by variation in the amount and diversity of leachate. Linear regression and correlation analyses indicated that leachate diversity had a close association with microbial Shannon diversity and evenness, whereas leachate amount had a close association with microbial biomass C, total microbial biomass, bacterial biomass, enzyme activities, and abundance of microbial groups. An ordinary least squares multiple regression and the structural equation model demonstrated that leachate amount had a greater effect on microbial biomass than leachate diversity, which had a greater impact on microbial Shannon diversity and evenness.

Conclusions

Our results indicate that plant diversity drives changes in soil microbial communities by altering the amount and diversity of leachate in the soil. The diversity of soil leachate determined the diversity of the microbial community to some extent.

Keywords

Soil leachate Plant richness Microbial diversity Biomass Grass species 

Notes

Acknowledgements

This work was financially supported by the National Natural Sciences Foundation of China (41771554), and National Key Research and Development Program of China (2016YFC0501707).

Supplementary material

11104_2019_4032_MOESM1_ESM.doc (139 kb)
ESM 1 (DOC 139 kb)

References

  1. 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.  https://doi.org/10.1074/jbc.M112.433300 CrossRefGoogle Scholar
  2. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681.  https://doi.org/10.1119/1.2338550 CrossRefGoogle Scholar
  3. Brzezinska MS, Lalke-Porczyk E, Donderski W, Walczak M (2009) Degradation of chitin in natural environment: role of actinomycetes. Pol J Ecol 57:229–238Google Scholar
  4. Chaparro JM, Badri DV, Vivanco JM (2014) Rhizosphere microbiome assemblage is affected by plant development. ISME J 8:790–803.  https://doi.org/10.1038/ismej.2013.196 CrossRefGoogle Scholar
  5. Cline LC, Hobbie SE, Madritch MD, Buyarski CR, Tilman D, Cavender-Bares JM (2018) Resource availability underlies the plant-fungal diversity relationship in a grassland ecosystem. Ecology 99:204–216.  https://doi.org/10.1002/ecy.2075 CrossRefGoogle Scholar
  6. Conant RT, Dalla-Betta P, Klopatek CC, Klopatek JA (2004) Controls on soil respiration in semiarid soils. Soil Biol Biochem 36:945–951.  https://doi.org/10.1016/j.soilbio.2004.02.013 CrossRefGoogle Scholar
  7. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327.  https://doi.org/10.1111/j.1574-6941.2010.00860.x CrossRefGoogle Scholar
  8. Eilers KG, Lauber CL, Knight R, Fierer N (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem 42:896–903.  https://doi.org/10.1016/j.soilbio.2010.02.003 CrossRefGoogle Scholar
  9. Eisenhauer N, Bessler H, Engels C, Gleixner G, Habekost M, Milcu A, Partsch S, Sabais ACW, 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.  https://doi.org/10.1890/08-2338.1 CrossRefGoogle Scholar
  10. Eisenhauer N, Lanoue A, Strecker T, Scheu S, Steinauer K, Thakur MP, Mommer L (2017) Root biomass and exudates link plant diversity with soil bacterial and fungal biomass. Sci Rep 7.  https://doi.org/10.1038/srep44641
  11. Fiehn O, Wohlgemuth G, Scholz M, Kind T, Lee DY, Lu Y, Moon S, Nikolau B (2008) Quality control for plant metabolomics: reporting MSI-compliant studies. Plant J 53:691–704.  https://doi.org/10.1111/j.1365-313X.2007.03387.x CrossRefGoogle Scholar
  12. Frostegard A, Tunlid A, Baath E (1993) Phospholipid fatty-acid composition, biomass, and activity of microbial communities from 2 soil types experimentally exposed to different heavy-metals. Appl Environ Microbiol 59:3605–3617Google Scholar
  13. Fusconi A (2014) Regulation of root morphogenesis in arbuscular mycorrhizae: what role do fungal exudates, phosphate, sugars and hormones play in lateral root formation? Ann Bot 113:19–33.  https://doi.org/10.1093/aob/mct258 CrossRefGoogle Scholar
  14. Grace JB (2006) Structural equation modeling natural systems. Cambridge University Press, New York, NYCrossRefGoogle Scholar
  15. Haichar FZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80.  https://doi.org/10.1016/j.soilbio.2014.06.017 CrossRefGoogle Scholar
  16. Janusz G, Pawlik A, Sulej J, Swiderska-Burek U, Jarosz-Wilkolazka A, Paszczynski A (2017) Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev 41:941–962.  https://doi.org/10.1093/femsre/fux049 CrossRefGoogle Scholar
  17. Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil—V: a method for measuring soil biomass. Soil Biol Biochem 8:209–213.  https://doi.org/10.1016/0038-0717(76)90005-5 CrossRefGoogle Scholar
  18. Kamilova F, Kravchenko LV, Shaposhnikov AI, Makarova N, Lugtenberg B (2006) Effects of the tomato pathogen Fusarium oxysporum f. Sp radicis-lycopersici and of the biocontrol bacterium Pseudomonas fluorescens WCS365 on the composition of organic acids and sugars in tomato root exudate. Mol Plant-Microbe Interact 19:1121–1126.  https://doi.org/10.1094/mpmi-19-1121 CrossRefGoogle Scholar
  19. Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5:588–595.  https://doi.org/10.1038/nclimate2580 CrossRefGoogle Scholar
  20. Khlifa R, Paquette A, Messier C, Reich PB, Munson AD (2017) Do temperate tree species diversity and identity influence soil microbial community function and composition? Ecology and Evolution 7:7965–7974.  https://doi.org/10.1002/ece3.3313 CrossRefGoogle Scholar
  21. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept & review. Soil Biol Biochem 83:184–199.  https://doi.org/10.1016/j.soilbio.2015.01.025 CrossRefGoogle Scholar
  22. Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vazquez PG, Malik AA, Roy J, Scheu S, Steinbeiss S, Thomson BC, Trumbore SE, Gleixner G (2015) Plant diversity increases soil microbial activity and soil carbon storage. Nat Commun 6.  https://doi.org/10.1038/ncomms7707
  23. Lorenzo P, Pereira CS, Rodriguez-Echeverria S (2013) Differential impact on soil microbes of allelopathic compounds released by the invasive Acacia dealbata link. Soil Biol Biochem 57:156–163.  https://doi.org/10.1016/j.soilbio.2012.08.018 CrossRefGoogle Scholar
  24. Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577.  https://doi.org/10.1128/mmbr.66.3.506-577.2002 CrossRefGoogle Scholar
  25. Makarova LE, Dudareva LV, Petrova IG, Vasil'eva GG (2016) Secretion of phenolic compounds into root exudates of pea seedlings upon inoculation with rhizobium leguminosarum bv. Viceae or Pseudomonas siringae pv. Pisi. Appl Biochem Microbiol 52:205–209.  https://doi.org/10.1134/s0003683816020095 CrossRefGoogle Scholar
  26. Mallik AU, Biswas SR, Siegwart CLC (2016) Belowground interactions between Kalmia angustifolia and Picea mariana: roles of competition, root exudates and ectomycorrhizal association. Plant Soil 403:471–483.  https://doi.org/10.1007/s11104-016-2819-z CrossRefGoogle Scholar
  27. Mellado-Vazquez PG, Lange M, Bachmann D, Gockele A, Karlowsky S, Milcu A, Piel C, Roscher C, Roy J, Gleixner G (2016) Plant diversity generates enhanced soil microbial access to recently photosynthesized carbon in the rhizosphere. Soil Biol Biochem 94:122–132.  https://doi.org/10.1016/j.soilbio.2015.11.012 CrossRefGoogle Scholar
  28. Mommer L, Padilla FM, van Ruijven J, de Caluwe H, Smit-Tiekstra A, Berendse F, de Kroon H (2015) Diversity effects on root length production and loss in an experimental grassland community. Funct Ecol 29:1560–1568.  https://doi.org/10.1111/1365-2435.12466 CrossRefGoogle Scholar
  29. Mommer L, van Ruijven J, de Caluwe H, Smit-Tiekstra AE, Wagemaker CAM, Ouborg NJ, Bogemann GM, van der Weerden GM, Berendse F, de Kroon H (2010) Unveiling below-ground species abundance in a biodiversity experiment: a test of vertical niche differentiation among grassland species. J Ecol 98:1117–1127.  https://doi.org/10.1111/j.1365-2745.2010.01702.x CrossRefGoogle Scholar
  30. Mueller KE, Tilman D, Fornara DA, Hobbie SE (2013) Root depth distribution and the diversity-productivity relationship in a long-term grassland experiment. Ecology 94:787–793.  https://doi.org/10.1890/12-1399.1 CrossRefGoogle Scholar
  31. Murugan R, Beggi F, Kumar S (2014) Belowground carbon allocation by trees, understory vegetation and soil type alter microbial community composition and nutrient cycling in tropical Eucalyptus plantations. Soil Biol Biochem 76:257–267.  https://doi.org/10.1016/j.soilbio.2014.05.022 CrossRefGoogle Scholar
  32. Neumann G, Bott S, Ohler MA, Mock HP, Lippmann R, Grosch R, Smalla K (2014) Root exudation and root development of lettuce (Lactuca sativa L. cv. Tizian) as affected by different soils. Front Microbiol 5.  https://doi.org/10.3389/fmicb.2014.00002
  33. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799.  https://doi.org/10.1038/nrmicro3109 CrossRefGoogle Scholar
  34. Ravenek JM, Bessler H, Engels C, Scherer-Lorenzen M, Gessler A, Gockele A, De Luca E, Temperton VM, Ebeling A, Roscher C, Schmid B, Weisser WW, Wirth C, de Kroon H, Weigelt A, Mommer L (2014) Long-term study of root biomass in a biodiversity experiment reveals shifts in diversity effects over time. Oikos 123:1528–1536.  https://doi.org/10.1111/oik.01502 CrossRefGoogle Scholar
  35. Read DB, Bengough AG, Gregory PJ, Crawford JW, Robinson D, Scrimgeour CM, Young IM, Zhang K, Zhang X (2003) Plant roots release phospholipid surfactants that modify the physical and chemical properties of soil. New Phytol 157:315–326.  https://doi.org/10.1046/j.1469-8137.2003.00665.x CrossRefGoogle Scholar
  36. Sana TR, Fischer S, Wohlgemuth G, Katrekar A, Jung K-h, Ronald PC, Fiehn O (2010) Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. Oryzae. Metabolomics 6:451–465.  https://doi.org/10.1007/s11306-010-0218-7 CrossRefGoogle Scholar
  37. Sauheitl L, Glaser B, Dippold M, Leiber K, Weigelt A (2010) Amino acid fingerprint of a grassland soil reflects changes in plant species richness. Plant Soil 334:353–363.  https://doi.org/10.1007/s11104-010-0387-1 CrossRefGoogle Scholar
  38. Schermelleh-Engel K, Moosbrugger H, Müller H (2003) Evaluating the fit of structural equation models: tests of significance and descriptive goodness-of-fit measures. Methods of Psychological Research Online 8:23–74Google Scholar
  39. Semchenko M, Saar S, Lepik A (2014) Plant root exudates mediate neighbour recognition and trigger complex behavioural changes. New Phytol 204:631–637.  https://doi.org/10.1111/nph.12930 CrossRefGoogle Scholar
  40. Spehn EM, Joshi J, Schmid B, Alphei J, Korner C (2000) Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 224:217–230.  https://doi.org/10.1023/a:1004891807664 CrossRefGoogle Scholar
  41. Spohn M, Kuzyakov Y (2013) Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation - coupling soil zymography with C-14 imaging. Soil Biol Biochem 67:106–113.  https://doi.org/10.1016/j.soilbio.2013.08.015 CrossRefGoogle Scholar
  42. Steinauer K, Chatzinotas A, Eisenhauer N (2016) Root exudate cocktails: the link between plant diversity and soil microorganisms? Ecology and Evolution 6:7387–7396.  https://doi.org/10.1002/ece3.2454 CrossRefGoogle Scholar
  43. Steinauer K, Tilman D, Wragg PD, Cesarz S, Cowles JM, Pritsch K, Reich PB, Weisser WW, Eisenhauer N (2015) Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment. Ecology 96:99–112.  https://doi.org/10.1890/14-0088.1 CrossRefGoogle Scholar
  44. Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998.  https://doi.org/10.1046/j.1365-2745.2000.00510.x CrossRefGoogle Scholar
  45. Thakur MP, Milcu A, Manning P, Niklaus PA, Roscher C, Power S, Reich PB, Scheu S, Tilman D, Ai F, Guo H, Ji R, Pierce S, Ramirez NG, Richter AN, Steinauer K, Strecker T, Vogel A, Eisenhauer N (2015) Plant diversity drives soil microbial biomass carbon in grasslands irrespective of global environmental change factors. Glob Chang Biol 21:4076–4085.  https://doi.org/10.1111/gcb.13011 CrossRefGoogle Scholar
  46. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707.  https://doi.org/10.1016/0038-0717(87)90052-6 CrossRefGoogle Scholar
  47. Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633.  https://doi.org/10.1126/science.1094875 CrossRefGoogle Scholar
  48. Yang RX, Gao ZG, Liu X, Yao Y, Cheng Y, Huang J, McDermott MI (2015) Effects of phenolic compounds of muskmelon root exudates on growth and pathogenic gene expression of Fusarium oxysporum f. Sp melonis. Allelopath J 35:175–185Google Scholar
  49. Yuan YS, Zhao WQ, Xiao J, Zhang ZL, Qiao MF, Liu Q, Yin HJ (2017) Exudate components exert different influences on microbially mediated C losses in simulated rhizosphere soils of a spruce plantation. Plant Soil 419:127–140.  https://doi.org/10.1007/s11104-017-3334-6 CrossRefGoogle Scholar
  50. Zhang C, Liu G, Song Z, Wang J, Guo L (2018) Interactions of soil bacteria and fungi with plants during long-term grazing exclusion in semiarid grasslands. Soil Biol Biochem 124:47–58.  https://doi.org/10.1016/j.soilbio.2018.05.026 CrossRefGoogle Scholar
  51. Zhang C, Liu G, Xue S, Song Z (2011) Rhizosphere soil microbial activity under different vegetation types on the loess plateau, China. Geoderma 161:115–125.  https://doi.org/10.1016/j.geoderma.2010.12.003 CrossRefGoogle Scholar
  52. Zhang C, Liu G, Xue S, Wang G (2015) Changes in rhizospheric microbial community structure and function during the natural recovery of abandoned cropland on the loess plateau, China. Ecol Eng 75:161–171.  https://doi.org/10.1016/j.ecoleng.2014.11.059 CrossRefGoogle Scholar
  53. Zhang J, Ai Z, Liang C, Wang G, Xue S (2017) Response of soil microbial communities and nitrogen thresholds of Bothriochloa ischaemum to short-term nitrogen addition on the loess plateau. Geoderma 308:112–119.  https://doi.org/10.1016/j.geoderma.2017.08.034 CrossRefGoogle Scholar
  54. Zhao J, Guo C, Tian C, Ma Y (2015) Heterologous expression and characterization of a GH3 beta-glucosidase from thermophilic Fungi Myceliophthora thermophila in Pichia pastoris. Appl Biochem Biotechnol 177:511–527.  https://doi.org/10.1007/s12010-015-1759-z CrossRefGoogle Scholar
  55. Zhu S, Vivanco JM, Manter DK (2016) Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107:324–333.  https://doi.org/10.1016/j.apsoil.2016.07.009 CrossRefGoogle Scholar
  56. Zwetsloot MJ, Kessler A, Bauerle TL (2018) Phenolic root exudate and tissue compounds vary widely among temperate forest tree species and have contrasting effects on soil microbial respiration. New Phytol 218:530–541.  https://doi.org/10.1111/nph.15041 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Chao Zhang
    • 1
  • Jie Wang
    • 1
  • Guobin Liu
    • 1
    • 2
  • Zilin Song
    • 3
  • Linchuan Fang
    • 1
    Email author
  1. 1.State Key Laboratory of Soil Erosion and Dryland Farming on the Loess PlateauNorthwest A&F UniversityYanglingPeople’s Republic of China
  2. 2.Institute of Soil and Water ConservationChinese Academy of Sciences and Ministry of Water ResourcesYanglingPeople’s Republic of China
  3. 3.College of Natural Resources and EnvironmentNorthwest A&F UniversityYanglingPeople’s Republic of China

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