Skip to main content

Advertisement

Log in

Plant Biomass and Soil Nutrients Mainly Explain the Variation of Soil Microbial Communities During Secondary Succession on the Loess Plateau

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Soil microorganisms play an important role in the circulation of materials and nutrients between plants and soil ecosystems, but the drivers of microbial community composition and diversity remain uncertain in different vegetation restoration patterns. We studied soil physicochemical properties (i.e., soil moisture, bulk density, pH, soil nutrients, available nutrients), plant characteristics (i.e., Shannon index [HPlant] and Richness index [SPlant], litter biomass [LB], and fine root biomass [FRB]), and microbial variables (biomass, enzyme activity, diversity, and composition of bacterial and fungal communities) in different plant succession patterns (Robinia pseudoacacia [MF], Caragana korshinskii [SF], and grassland [GL]) on the Loess Plateau. The herb communities, soil microbial biomass, and enzyme activities were strongly affected by vegetation restoration, and soil bacterial and fungal communities were significantly different from each other at the sites. Correlation analysis showed that LB and FRB were significantly positively correlated with the Chao index of soil bacteria, soil microbial biomass, enzyme activities, Proteobacteria, Zygomycota, and Cercozoa, while negatively correlated with Actinobacteria and Basidiomycota. In addition, soil water content (SW), pH, and nutrients have important effects on the bacterial and fungal diversities, as well as Acidobacteria, Proteobacteria, Actinobacteria, Nitrospirae, Zygomycota, and microbial biomass. Furthermore, plant characteristics and soil properties modulated the composition and diversity of soil microorganisms, respectively. Overall, the relative contribution of vegetation and soil to the diversity and composition of soil bacterial and fungal communities illustrated that plant characteristics and soil properties may synergistically modulate soil microbial communities, and the composition and diversity of soil bacterial and fungal communities mainly depend on plant biomass and soil nutrients.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data Availability

Some or all data, models, or code generated or used during the study are available from the corresponding author by request.

References

  1. Zhang C, Liu G, Xue S, Wang G (2016) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biology & Biochemistry 97:40–49. https://doi.org/10.1016/j.soilbio.2016.02.013

    Article  CAS  Google Scholar 

  2. Zhong Z, Wang X, Zhang X, Zhang W, Xu Y, Ren C, Han X, Yang G (2019) Edaphic factors but not plant characteristics mainly alter soil microbial properties along a restoration chronosequence of Pinus tabulaeformis stands on Mt. Ziwuling, China. Forest Ecology and Management:453. https://doi.org/10.1016/j.foreco.2019.117625

  3. Wu X, Xu H, Tuo D, Wang C, Fu B, Lv Y, Liu G (2020) Land use change and stand age regulate soil respiration by influencing soil substrate supply and microbial community. Geoderma 359:113991. https://doi.org/10.1016/j.geoderma.2019.113991

    Article  CAS  Google Scholar 

  4. Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biology and Fertility of Soils 45:115–131. https://doi.org/10.1007/s00374-008-0334-y

    Article  Google Scholar 

  5. Brockett BFT, Prescott CE, Grayston SJ (2012) Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biology & Biochemistry 44:9–20. https://doi.org/10.1016/j.soilbio.2011.09.003

    Article  CAS  Google Scholar 

  6. Ren C, Zhang W, Zhong Z, Han X, Yang G, Feng Y, Ren G (2018) Differential responses of soil microbial biomass, diversity, and compositions to altitudinal gradients depend on plant and soil characteristics. Science of the Total Environment 610:750–758. https://doi.org/10.1016/j.scitotenv.2017.08.110

    Article  CAS  Google Scholar 

  7. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11:296–310. https://doi.org/10.1111/j.1461-0248.2007.01139.x

    Article  PubMed  Google Scholar 

  8. Xu M, Lu X, Xu Y, Zhong Z, Zhang W, Ren C, Han X, Yang G, Feng Y (2020) Dynamics of bacterial community in litter and soil along a chronosequence of Robinia pseudoacacia plantations. Science of the Total Environment 703:135613. https://doi.org/10.1016/j.scitotenv.2019.135613

    Article  CAS  Google Scholar 

  9. Drenovsky RE, Steenwerth KL, Jackson LE, Scow KM (2010) Land use and climatic factors structure regional patterns in soil microbial communities. Global Ecology and Biogeography 19:27–39. https://doi.org/10.1111/j.1466-8238.2009.00486.x

    Article  PubMed  PubMed Central  Google Scholar 

  10. Prescott CE, Grayston SJ (2013) Tree species influence on microbial communities in litter and soil: current knowledge and research needs. Forest Ecology and Management 309:19–27. https://doi.org/10.1016/j.foreco.2013.02.034

    Article  Google Scholar 

  11. Yang Y, Cheng H, Dou Y, An S (2020) Plant and soil traits driving soil fungal community due to tree plantation on the Loess Plateau. Science of the Total Environment 708:134560. https://doi.org/10.1016/j.scitotenv.2019.134560

    Article  CAS  Google Scholar 

  12. Liu J, Yang Z, Dang P, Zhu H, Gao Y, Vu Ngoc H, Zhao Z (2018) Response of soil microbial community dynamics to Robinia pseudoacacia L. afforestation in the loess plateau: a chronosequence approach. Plant and Soil 423:327–338. https://doi.org/10.1007/s11104-017-3516-2

    Article  CAS  Google Scholar 

  13. Reinhart KO, Dangi SR, Vermeire LT (2016) The effect of fire intensity, nutrients, soil microbes, and spatial distance on grassland productivity. Plant and Soil 409:203–216. https://doi.org/10.1007/s11104-016-2957-3

    Article  CAS  Google Scholar 

  14. Carrino-Kyker SR, Kluber LA, Petersen SM, Coyle KP, Hewins CR, DeForest JL, Smemo KA, Burke DJ (2016) Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests. Fems Microbiology Ecology 92. https://doi.org/10.1093/femsec/fiw024

  15. Holste EK, Kobe RK (2017) Tree species and soil nutrients drive tropical reforestation more than associations with mycorrhizal fungi. Plant and Soil 410:283–297. https://doi.org/10.1007/s11104-016-3013-z

    Article  CAS  Google Scholar 

  16. Zhou Z, Wang C, Luo Y (2018) Effects of forest degradation on microbial communities and soil carbon cycling: a global meta-analysis. Global Ecology and Biogeography 27:110–124. https://doi.org/10.1111/geb.12663

    Article  Google Scholar 

  17. Gebhardt M, Fehmi JS, Rasmussen C, Gallery RE (2017) Soil amendments alter plant biomass and soil microbial activity in a semi-desert grassland. Plant and Soil 419:53–70. https://doi.org/10.1007/s11104-017-3327-5

    Article  CAS  Google Scholar 

  18. Li S, Shakoor A, Wubet T, Zhang N, Liang Y, Ma K (2018) Fine-scale variations of fungal community in a heterogeneous grassland in Inner Mongolia: effects of the plant community and edaphic parameters. Soil Biology & Biochemistry 122:104–110. https://doi.org/10.1016/j.soilbio.2018.04.007

    Article  CAS  Google Scholar 

  19. Zhang W, Xu Y, Gao D, Wang X, Liu W, Deng J, Han X, Yang G, Feng Y, Ren G (2019) Ecoenzymatic stoichiometry and nutrient dynamics along a revegetation chronosequence in the soils of abandoned land and Robinia pseudoacacia plantation on the Loess Plateau, China. Soil Biology & Biochemistry 134:1–14. https://doi.org/10.1016/j.soilblo.2019.03.017

    Article  Google Scholar 

  20. Ren C, Zhao F, Shi Z, Chen J, Han X, Yang G, Feng Y, Ren G (2017) Differential responses of soil microbial biomass and carbon-degrading enzyme activities to altered precipitation. Soil Biology & Biochemistry 115:1–10. https://doi.org/10.1016/j.soilbio.2017.08.002

    Article  CAS  Google Scholar 

  21. Xu Y, Zhong Z, Zhang W, Han X, Yang G, Ren C, Feng Y, Ren G, Wang X (2019) Responses of soil nosZ-type denitrifying microbial communities to the various land-use types of the Loess Plateau, China. Soil & Tillage Research 195:104378. https://doi.org/10.1016/j.still.2019.104378

    Article  Google Scholar 

  22. Ren C, Zhao F, Kang D, Yang G, Han X, Tong X, Feng Y, Ren G (2016) Linkages of C:N:P stoichiometry and bacterial community in soil following afforestation of former farmland. Forest Ecology and Management 376:59–66. https://doi.org/10.1016/j.foreco.2016.06.004

    Article  Google Scholar 

  23. Zhao F, Zhang L, Ren C, Sun J, Han X, Yang G, Wang J (2016) Effect of microbial carbon, nitrogen, and phosphorus stoichiometry on soil carbon fractions under a black locust forest within the central Loess Plateau of China. Soil Science Society of America Journal 80:1520–1530. https://doi.org/10.2136/sssaj2016.06.0175

    Article  CAS  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. Liu X, Zhang S (2019) Nitrogen addition shapes soil enzyme activity patterns by changing pH rather than the composition of the plant and microbial communities in an alpine meadow soil. Plant and Soil 440:11–24. https://doi.org/10.1007/s11104-019-04054-5

    Article  CAS  Google Scholar 

  26. Zhang W, Ren C, Deng J, Zhao F, Yang G, Tong X, Feng Y, Han X (2018) Plant functional composition and species diversity affect soil C, N, and P during secondary succession of abandoned farmland on the Loess Plateau. Ecological Engineering 122:91–99. https://doi.org/10.1016/j.ecoleng.2018.07.031

    Article  Google Scholar 

  27. Bao S (2000) Soil and agricultural chemistry analysis. China agriculture press, Beijing, China (in Chinese)

    Google Scholar 

  28. Xu Z, Yu G, Zhang X, He N, Wang Q, Wang S, Wang R, Zhao N, Jia Y, Wang C (2017) Soil enzyme activity and stoichiometry in forest ecosystems along the North-South Transect in eastern China (NSTEC). Soil Biology & Biochemistry 104:152–163. https://doi.org/10.1016/j.soilbio.2016.10.020

    Article  CAS  Google Scholar 

  29. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation. Microbiological Reviews 59:143–169. https://doi.org/10.1128/mmbr.59.1.143-169.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Xu L, Ravnskov S, Larsen J, Nilsson RH, Nicolaisen M (2012) Soil fungal community structure along a soil health gradient in pea fields examined using deep amplicon sequencing. Soil Biology & Biochemistry 46:26–32. https://doi.org/10.1016/j.soilbio.2011.11.010

    Article  CAS  Google Scholar 

  32. Meier E, Paal J, Liira J, Juriado I (2005) Influence of tree stand age and management on the species diversity in Estonian eutrophic alvar and boreo-nemoral Pinus sylvestris forests. Scandinavian Journal of Forest Research 20:135–144. https://doi.org/10.1080/14004080510042155

    Article  Google Scholar 

  33. Zhang P, Li B, Wu J, Hu S (2019) Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecology Letters 22:200–210. https://doi.org/10.1111/ele.13181

    Article  PubMed  Google Scholar 

  34. Spohn M, Kuzyakov Y (2014) Spatial and temporal dynamics of hotspots of enzyme activity in soil as affected by living and dead roots-a soil zymography analysis. Plant and Soil 379:67–77. https://doi.org/10.1007/s11104-014-2041-9

    Article  CAS  Google Scholar 

  35. Cui Y, Fang L, Guo X, Wang X, Zhang Y, Li P, Zhang X (2018) Ecoenzymatic stoichiometry and microbial nutrient limitation in rhizosphere soil in the arid area of the northern Loess Plateau, China. Soil Biology & Biochemistry 116:11–21. https://doi.org/10.1016/j.soilbio.2017.09.025

    Article  CAS  Google Scholar 

  36. Peng X, Wang W (2016) Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biology & Biochemistry 98:74–84. https://doi.org/10.1016/j.soilbio.2016.04.008

    Article  CAS  Google Scholar 

  37. Zhang F-G, Zhang Q-G (2016) Microbial diversity limits soil heterotrophic respiration and mitigates the respiration response to moisture increase. Soil Biology & Biochemistry 98:180–185. https://doi.org/10.1016/j.soilbio.2016.04.017

    Article  CAS  Google Scholar 

  38. Canals RM, Mugica L, Duran M, San Emeterio L (2019) Soil bacterial functional diversity mirrors the loss of plant diversity by the expansion of a native tall-grass in high mountain grasslands. Plant and Soil 445:243–257. https://doi.org/10.1007/s11104-019-04281-w

    Article  CAS  Google Scholar 

  39. Uibopuu A, Moora M, Oepik M, Zobel M (2012) Temperate forest understorey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant and Soil 356:331–339. https://doi.org/10.1007/s11104-011-1116-0

    Article  CAS  Google Scholar 

  40. Xiang X, Gibbons SM, Yang J, Kong J, Sun R, Chu H (2015) Arbuscular mycorrhizal fungal communities show low resistance and high resilience to wildfire disturbance. Plant and Soil 397:347–356. https://doi.org/10.1007/s11104-015-2633-z

    Article  CAS  Google Scholar 

  41. Bauer JT, Blumenthal N, Miller AJ, Ferguson JK, Reynolds HL (2017) Effects of between-site variation in soil microbial communities and plant-soil feedbacks on the productivity and composition of plant communities. Journal of Applied Ecology 54:1028–1039. https://doi.org/10.1111/1365-2664.12937

    Article  CAS  Google Scholar 

  42. Chen CR, Xu ZH, Blumfield TJ, Hughes JM (2003) Soil microbial biomass during the early establishment of hoop pine plantation: seasonal variation and impacts of site preparation. Forest Ecology and Management 186:213–225. https://doi.org/10.1016/s0378-1127(03)00275-5

    Article  Google Scholar 

  43. Wang K, Zhang Y, Tang Z, Shangguan Z, Chang F, Fa J, Chen Y, He X, Shi W, Deng L (2019) Effects of grassland afforestation on structure and function of soil bacterial and fungal communities. Science of the Total Environment 676:396–406. https://doi.org/10.1016/j.scitotenv.2019.04.259

    Article  CAS  Google Scholar 

  44. Merrick MJ, Edwards RA (1995) Nitrogen control in bacteria. Microbiological Reviews 59: 604-&. https://doi.org/10.1128/mmbr.59.4.604-622.1995

  45. Marzluf GA (1997) Genetic regulation of nitrogen metabolism in the fungi. Microbiology and Molecular Biology Reviews 61:17. https://doi.org/10.1128/.61.1.17-32.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Barak P, Jobe BO, Krueger AR, Peterson LA, Laird DA (1997) Effects of long-term soil acidification due to nitrogen fertilizer inputs in Wisconsin. Plant and Soil 197:61–69. https://doi.org/10.1023/a:1004297607070

    Article  CAS  Google Scholar 

  47. Drenovsky RE, Vo D, Graham KJ, Scow KM (2004) Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microbial Ecology 48:424–430. https://doi.org/10.1007/s00248-003-1063-2

    Article  CAS  PubMed  Google Scholar 

  48. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology & Biochemistry 37:937–944. https://doi.org/10.1016/j.soilbio.2004.09.014

    Article  CAS  Google Scholar 

  49. Kyaschenko J, Clemmensen KE, Hagenbo A, Karltun E, Lindahl BD (2017) Shift in fungal communities and associated enzyme activities along an age gradient of managed Pinus sylvestris stands. Isme Journal 11:863–874. https://doi.org/10.1038/ismej.2016.184

    Article  CAS  Google Scholar 

Download references

Funding

Forest and Grass Technology Innovation Development and Research Project of the State Forestry and Grassland Administration (2020132111), Key project of Shaanxi Provincial Natural Science Foundation (2018JZ4002) and Shaanxi Engineering Research Center of Circular Agriculture (2019HBGC-13) financially supported this work.

Author information

Authors and Affiliations

Authors

Contributions

MPX, XHH and JYW conceived and designed the experiments; MPX and CJR performed the experiments and processed the samples; MPX wrote a first version of the manuscript, and YFZ and GHY substantially contributed to the last version of the manuscript.

Corresponding author

Correspondence to Xin-hui Han.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Supplementary Information

ESM 1

(DOCX 487 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Mp., Wang, Jy., Zhu, Yf. et al. Plant Biomass and Soil Nutrients Mainly Explain the Variation of Soil Microbial Communities During Secondary Succession on the Loess Plateau. Microb Ecol 83, 114–126 (2022). https://doi.org/10.1007/s00248-021-01740-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-021-01740-9

Keywords

Navigation