Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Soil properties and microbial communities are the main contributors to aboveground vegetative biomass in reseeded grassland after long-term growth

  • 80 Accesses



The overall production of degraded grassland ecosystems can be improved by reseeding appropriate species, but the responses of soil microbes to reseeded grassland after a long-term growth, especially the mediation effects of soil chemical compounds on the soil microbial community composition, have rarely been reported.

Materials and methods

In this study, we reseeded a degraded grassland with Bromus inermis Leyss and investigated the changes in aboveground (grassland biomass) and belowground factors (soil properties, soil chemical compounds, soil microbial diversity, and community) under reseeded and non-reseeded treatments.

Results and discussion

The reseeding of B. inermis significantly (P < 0.05) enchacecd the aboveground vegetative biomass by 22.72% as compared with the plots that were not reseeded. Significant (P < 0.05) differences were also observed in the soil chemical compounds and microbial diversity and community between the reseeded and non-reseeded treatments. Soil bacterial (R2 = 0.6271, P = 0.0007) and fungal α-diversity (R2 = 0.5895, P = 0.0013) were both positively correlated with grassland biomass. Moreover, the community compositons of soil bacterial (R = 0.465, P = 0.002) and fungal (R = 0.720, P = 0.001) also had significant correlations with grassland biomass. Actinoplanes, Streptomyces, Bacillus, and Mesorhizobium were identified as potential agents for promoting grassland growth. Network analysis showed that the assemblages of soil microbes in the reseeding treatment formed larger and more complex networks than those in the non-reseeding treatment.


Our study, cutting in terms of soil microbial ecology, provides a valuable model for explaining the aboveground responses to the establishment of perennial grass species in degraded grasslands.

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

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

Data accessibility

The raw sequence data were deposited in the National Center for Biotechnology Information (NCBI) under accession numbers SRP133594 (bacterial 16S RNA) and SRP133597 (fungal ITS), respectively.


  1. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

  2. Baer SG, Kitchen DJ, Blair JM, Rice CW (2002) Changes in ecosystem structure and function along a chronosequence of restored grasslands. Ecol Appl 12:1688–1701

  3. Bai YF, Han XG, Wu JG, Chen ZZ, Li LH (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431(9):181–184

  4. Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160

  5. Bhatia S, Dubey RC, Maheshwari DK (2003) Antagonistic effect of fluorescent pseudomonads against Macrophomina phaseolina that causes charcoal rot of ground nut. Indian J Exp Biol 41:1441–1446

  6. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522

  7. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992

  8. Chaer G, Fernandes M, Myrold D, Bottomley P (2009) Comparative resistance and resilience of soil microbial communities and enzyme activities in adjacent native forest and agricultural soils. Microb Ecol 58:414–424

  9. Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48(5):489–499

  10. Chen YF, Tang Z, Li H, Han XM, Li YF, Hu C (2014) Research progress on ecosystem complexity-stability relationships based on soil food web. Acta Ecol Sin 34(9):2173–2186

  11. Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB (2006) Diverse responses of phenology to global changes in a grassland ecosystem. Proc Natl Acad Sci U S A 103(37):13740–13744

  12. Davidson AD, Ponce E, Lightfoot DC, Fredrickson EL, Brown JH, Cruzado J, Ceballos G (2010) Rapid response of a grassland ecosystem to an experimental manipulation of a keystone rodent and domestic livestock. Ecology 91(11):3189–3200

  13. Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J (2012) Molecular ecological network analyses. BMC Bioinformatics 13:113

  14. Dobson AP, Bradshaw AD, Baker JM (1997) Hopes for the future: restoration ecology and conservation biology. Science 277:515–522

  15. Dupont YL, Olesen JM (2009) Ecological modules and roles of species in heathland plant-insect flower visitor networks. J Anim Ecol 78:346–353

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

  17. Eltarabily KA (2003) An endophytic chitinase-producing isolate of Actinoplanes missouriensis, with potential for biological control of root rot of lupin caused by Plectosporium tabacinum. Aust J Bot 51(3):257–266

  18. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550

  19. Fliessbach A, Oberholzer HR, Gunst L, Mader P (2007) Soil organic matter and biological soil quality indicators after 21 years of organic and conventional farming. Agric Ecosyst Environ 118:273–284

  20. Garbeva P, van Elsas JD, van Veen JA (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302(1–2):19–32

  21. Gaume A, Machler F, Frossard E (2001) Aluminum resistance in two cultivars of Zea mays L.: root exudation of organic acids and influence of phosphorus nutrition. Plant Soil 234(1):73–81

  22. Gebhart DL, Johnson HB, Mayeux HS, Polly HW (1994) The CRP increases soil organic carbon. J Soil Water Conserv 49:488–492

  23. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

  24. Guimera R, Amaral L (2005) Functional cartography of complex metabolic networks. Nature 433:895–900

  25. Gupta CP, Dubey RC, Maheshwari DK (2002) Plant growth enhancement and suppression of Macrophomina phaseolina causing charcoal rot of peanut by fluorescent Pseudomonas. Biol Fert Soils 35:399–405

  26. Haas D, Keel D (2003) Regulation of antibiotic production in root colonizing Pseudomonas spp. and relevance for biological control of plant diseases. Annu Rev Phytopathol 41:117–153

  27. Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–190

  28. Hollister EB, Hu P, Wang AS, Hons FM, Gentry TJ (2013) Differential impacts of brassicaceous and nonbrassicaceous oilseed meals on soil bacterial and fungal communities. FEMS Microbiol Ecol 83:632–641

  29. Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165(4):397–407

  30. Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borriss R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148(7):2097–2109

  31. IUSS Working Group WRB (2015) World Reference Base for soil resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome

  32. Kamnev AA, Lelie D (2000) Chemical and biological parameters as tools to evaluate and improve heavy metal phytoremediation. Biosci Rep 20:239–258

  33. Killham K (1994) Soil ecology. Cambridge University Press, Cambridge

  34. Knops JMH, Tilman D (2000) Dynamics of soil nitrogen and carbon accumulation for 61 years after agricultural abandonment. Ecology 81:88–98

  35. Knudsen D, Peterson G, Pratt P (1982) Lithium, sodium, and potassium. In: Page AL, Miller RH, Kenney DR (eds) Methods of soil analysis, part 2, Chemical and Microbiological Properties. American Society of Agronomy, Soil Science Society of American, Madison, pp 225–246

  36. Liao C, Hochholdinger F, Li C (2012) Comparative analyses of three legume species reveals conserved and unique root extracellular proteins. Proteomics 12(21):3219–3228

  37. Ling N, Zhu C, Xue C, Duan YH, Peng C, Guo SW, Shen QR (2016) Insight into how organic amendments can shape the soil microbiome in long-term field experiments as revealed by network analysis. Soil Biol Biochem 99:137–149

  38. Lu L, Yin S, Liu X, Zhang W, Gu T, Shen QR, Qiu HZ (2013) Fungal networks in yield-invigorating and -debilitating soils induced by prolonged potato monoculture. Soil Biol Biochem 65:186–194

  39. Mason HE, Spaner D (2006) Competitive ability of wheat in conventional and organic management systems: a review of the literature. Can J Plant Sci 86:333–343

  40. Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332(6033):1097–1100

  41. Nair A, Ngouajio M (2012) Soil microbial biomass, functional microbial diversity, and nematode community structure as affected by cover crops and compost in an organic vegetable production system. Appl Soil Ecol 58:45–55

  42. Newbold T, Hudson LN, Hill SL, Contu S, Lysenko I, Senior RA, Purvis A (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50

  43. Newman M (2006) Modularity and community structure in networks. Proc Natl Acad Sci U S A 103:8577–8582

  44. Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Smernik RJ, Cavagnaro TR (2014) Does the chemical nature of soil carbon drive the structure and functioning of soil microbial communities? Soil Biol Biochem 70(2):54–61

  45. Olesen J, Bascompte J, Dupont Y, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci U S A 104:19891–19896

  46. Olsen SR, Sommers LE (1982) Phosphorous. In: Page AL et al (eds) Methods of soil analysis. Part 2, Agronomy, vol 9, 2nd edn. American Society of Agronomy, Madison, WI, pp 403–429

  47. Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mill LS, Robert TP (1996) Challenges in the quest for keystones. Bioscience 46:609–620

  48. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soil borne pathogens and beneficial microorganisms. Plant Soil 321:341–361

  49. Reeder JD, Schuman GE, Bowman RA (1998) Soil C and N changes on conservation reserve program lands in the Central Great Plains. Soil Tillage Res 47:339–349

  50. Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H (2012) Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28(4):1503–1509

  51. Samson FB, Knopf FL (1994) Prairie conservation in North America. BioScience 44:418–421

  52. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

  53. Scheffer M, Carpenter SR, Lenton TM, Bascompte J, Brock W, Dakos V, van de Koppel J, van de Leemput IA, Levin SA, Nes EH, van Pascual M, Vandermeer J (2012) Anticipating critical transitions. Science 338:344–348

  54. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541

  55. Shen ZZ, Ruan YZ, Chao X, Zhang J, Li R, Shen QR (2015) Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fert Soils 51(5):553–562

  56. Shi R (1996) Agricultural chemistry analyses of soils, second edn. China Agricultural Press, Beijing, China, pp 37–39 (in Chinese)

  57. Smith RS, Shiel R, Bardgett RD, Millward DP, Corkhill P, Rolph G, Peacock S (2003) Soil microbial community, fertility, vegetation and diversity as targets in the restoration management of a meadow grassland. J Appl Ecol 40(1):51–64

  58. Song Y, Zhu C, Raza W, Wang DS, Huang QW, Guo SW, Ling N, Shen QR (2016) Coupling of the chemical niche and microbiome in the rhizosphere: implications from watermelon grafting. Front Agric Sci Eng 3(3):249–262

  59. Sun H, Deng S, Raun W (2004) Bacterial community structure and diversity in a century-old manure-treated agroecosystem. Appl Environ Microbiol 70:5868–5874

  60. van der Heijden MG, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

  61. Viebahn M, Veenman C, Wernars K, van Loon LC, Smit E, Bakker PAHM (2005) Assessment of differences in ascomycete communities in the rhizosphere of field-grown wheat and potato. FEMS Microbiol Ecol 53(2):245–253

  62. 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 Microb 73:5261–5267

  63. Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30(1):159–163

  64. Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Sci Soc Am J 22:677–678

  65. Worm B, Duffy JE (2003) Biodiversity, productivity and stability in real food webs. Trends Ecol Evol 18(12):628–632

  66. Zahir ZA, Arshad M, Wtjr F (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168

  67. Zhang FG, Xu XX, Huo YQ, Xiao Y (2019) Trichoderma-inoculation and mowing synergistically altered soil available nutrients, rhizosphere chemical compounds and soil microbial community, potentially driving alfalfa growth. Front Microbiol 9:3241

  68. Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X (2010) Functional molecular ecological networks. mBio 1(4):e00169–e00110. https://doi.org/10.1128/mBio.00169-10

Download references


We thank G. W. Yang for his assistance in plant and soil sampling.


This work was financially supported by the earmarked fund for the China Agriculture Research System (CARS-34) and the Nanjing Agricultural University Foundation (Y0201600442).

Author information

Correspondence to Yan Xiao.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible editor: Yongtao Li

Electronic supplementary material


(DOCX 139 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhang, F., Xu, X., Shen, Z. et al. Soil properties and microbial communities are the main contributors to aboveground vegetative biomass in reseeded grassland after long-term growth. J Soils Sediments 20, 824–835 (2020). https://doi.org/10.1007/s11368-019-02433-0

Download citation


  • Bromus inermis Leyss
  • MiSeq sequencing
  • Soil chemical compounds
  • Soil bacterial and fungal community
  • Soil properties