Skip to main content

Advertisement

Log in

Physicochemical and Biotic Changes and the Phylogenetic Evenness of Microbial Community in Soil Subjected to Phytoreclamation

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

Abstract

Phytoreclamation is the intervention of plants to improve degraded soil quality, changing soil biotic and abiotic properties. Many studies have focused on microbial composition and bioactivity, but few explored the changes in phylogenetic assemblages of soil microbiota after phytoreclamation. This study compared microbiomes of bare land to those of planted soils and investigated how the rhizosphere environment affects microbial assemblages from monocot Poa pratensis and eudicot Dianthus plumarius plantings using 16S rRNA metabarcoding. The results showed that the biotic susceptibility of soil to the rhizosphere environment was higher than that of the abiotic. A noticeable change was in some soil physicochemical properties like Na, P, Zn, Cu, C, and sand-to-silt proportion before and after phytoreclamation, but not between the rhizosphere and bulk soil of plantings. Contrastingly, microbial composition and diversity were significantly affected by both turfing and rhizosphere effects and were more susceptible to differences in turfing or not than in planting species. In the turfgrass, the microbiome differences between plants were greater in the rhizosphere than in the surrounding bulk soil, indicating the proximal influence of root exudates. We also found that the main abiotic factors that influenced microbial composition were Na, Zn, NOx, N, and S; as for the phylogenetic assemblages, were by K levels and the increase of silt. Turfgrass decomposes soil aggregates and changes the physicochemical properties, thereby evens the phylogenetic clustering of the soil microbial community. We demonstrated that the deterministic process affects the microbial assemblage and acts as a selective agent of the soil microbiota in fundamental and realized niches. Phytoreclamation may lead to abiotic soil changes that reallocate resources to microbes. This could affect the phylogeny of the microbial assemblages and increase microbial richness.

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

Similar content being viewed by others

Availability of Data and Material

The obtained 16S rRNA metabarcoding sequences are deposited NCBI GenBank under the bioproject PRJNA732794 (accession number: SAMN19340935-SAMN19340984).

Code Availability

Not applicable.

References

  1. Guimarães BC, Arends JB, Van der Ha D, Van de Wiele T, Boon N, Verstraete W (2010) Microbial services and their management: recent progresses in soil bioremediation technology. Appl Soil Ecol 46:157–167

    Article  Google Scholar 

  2. Nielsen MN, Winding A (2002) Microorganisms as indicators of soil health. Ministry of the Environment, National Environmental Research Institute, Denmark

  3. Ferris H, Tuomisto H (2015) Unearthing the role of biological diversity in soil health. Soil Biol Biochem 85:101–109

    Article  CAS  Google Scholar 

  4. Pimentel D, Kounang N (1998) Ecology of soil erosion in ecosystems. Ecosystems 1:416–426

    Article  CAS  Google Scholar 

  5. Pimentel D, Harvey C, Resosudarmo P, Sinclair K, Kurz D, McNair M, Crist S, Shpritz L, Fitton L, Saffouri R (1995) Environmental and economic costs of soil erosion and conservation benefits. Science 267:1117–1123

    Article  CAS  Google Scholar 

  6. Veihe A, Hasholt B, Schiøtz IG (2003) Soil erosion in Denmark: processes and politics. Environ Sci Policy 6:37–50

    Article  Google Scholar 

  7. Prescott CE (2005) Decomposition and mineralization of nutrients from litter and humus. In: BassiriRad H (ed) Nutrient acquisition by plants: an ecological perspective. Springer, Berlin Heidelberg, pp 15–41

    Chapter  Google Scholar 

  8. Ullah A, Bano A, Khan N (2021) Climate change and salinity effects on crops and chemical communication between plants and plant growth-promoting microorganisms under stress. Front Sustain Food Syst 5:161. https://doi.org/10.3389/fsufs.2021.618092

    Article  Google Scholar 

  9. Nosetto MD, Jobbágy EG, Tóth T, Di Bella CM (2007) The effects of tree establishment on water and salt dynamics in naturally salt-affected grasslands. Oecologia 152:695–705. https://doi.org/10.1007/s00442-007-0694-2

    Article  Google Scholar 

  10. Wu Z, Sun L, Li Y, Sun Q (2020) Shifts in vegetation-associated microbial community in the reclamation of coal mining subsidence land. Environ Eng Sci 37:838–848. https://doi.org/10.1089/ees.2019.0491

    Article  CAS  Google Scholar 

  11. Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–339

    Article  CAS  Google Scholar 

  12. Hu L, Robert CA, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, Van Der Heijden MG (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:1–13

    Article  Google Scholar 

  13. Qadir M, Oster J (2002) Vegetative bioremediation of calcareous sodic soils: history, mechanisms, and evaluation. Irrig Sci 21:91–101

    Article  Google Scholar 

  14. Zhou ZC, Shangguan ZP, Zhao D (2006) Modeling vegetation coverage and soil erosion in the Loess Plateau Area of China. Ecol Model 198:263–268

    Article  Google Scholar 

  15. Zhang L, Wang J, Bai Z, Lv C (2015) Effects of vegetation on runoff and soil erosion on reclaimed land in an opencast coal-mine dump in a loess area. CATENA 128:44–53

    Article  Google Scholar 

  16. HilleRisLambers J, Adler PB, Harpole W, Levine JM, Mayfield MM (2012) Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43:227–248

    Article  Google Scholar 

  17. Ayangbenro AS, Babalola OO (2021) Reclamation of arid and semi-arid soils: the role of plant growth-promoting archaea and bacteria. Curr Plant Biol 25:100173. https://doi.org/10.1016/j.cpb.2020.100173

  18. Jorquera MA, Maruyama F, Ogram AV, Navarrete OU, Lagos LM, Inostroza NG, Acuña JJ, Rilling JI, de La Luz MM (2016) Rhizobacterial community structures associated with native plants grown in Chilean extreme environments. Microb Ecol 72:633–646. https://doi.org/10.1007/s00248-016-0813-x

    Article  CAS  Google Scholar 

  19. Shi S, Nuccio E, Herman DJ, Rijkers R, Estera K, Li J, da Rocha UN, He Z, Pett-Ridge J, Brodie EL, Zhou J, Firestone M (2015) Successional trajectories of rhizosphere bacterial communities over consecutive seasons. mBio 6:e00746-00715. https://doi.org/10.1128/mBio.00746-15

    Article  Google Scholar 

  20. Dong M, Kowalchuk GA, Liu H, Xiong W, Deng X, Zhang N, Li R, Shen Q, Dini-Andreote F (2021) Microbial community assembly in soil aggregates: a dynamic interplay of stochastic and deterministic processes. Appl Soil Ecol 163:103911. https://doi.org/10.1016/j.apsoil.2021.103911

  21. Huber P, Metz S, Unrein F, Mayora G, Sarmento H, Devercelli M (2020) Environmental heterogeneity determines the ecological processes that govern bacterial metacommunity assembly in a floodplain river system. ISME J 14:2951–2966. https://doi.org/10.1038/s41396-020-0723-2

    Article  Google Scholar 

  22. Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87:S100–S108

    Article  Google Scholar 

  23. Tripathi BM, Stegen JC, Kim M, Dong K, Adams JM, Lee YK (2018) Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J 12:1072–1083. https://doi.org/10.1038/s41396-018-0082-4

    Article  CAS  Google Scholar 

  24. Hoffmann C, Funk R, Reiche M, Li Y (2011) Assessment of extreme wind erosion and its impacts in Inner Mongolia, China. Aeol Res 3:343–351

    Article  Google Scholar 

  25. Yang Y-Z, Gao R-H, Luo M-X, Huang B-H, Liao P-C (2020) Tissue-specific bioaccumulation of heavy metals in Ammopiptanthus mongolicus, the only evergreen shrub in the desert of Northwest China. Taiwania 65:140–148. https://doi.org/10.6165/tai.2020.65.140

    Article  CAS  Google Scholar 

  26. Geological and Mineral Industry Standards of the People’s Republic of China (2016) Regional geochemical exploration sample analysis method. Ministry of Land and Resources of the People’s Republic of China, China

    Google Scholar 

  27. Ewing B, Green P (1998) Base-calling of automated sequencer traces using Phred. II. error probabilities. Genome Res 8:186–194. https://doi.org/10.1101/gr.8.3.186

    Article  CAS  Google Scholar 

  28. Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8:175–185. https://doi.org/10.1101/gr.8.3.175

    Article  CAS  Google Scholar 

  29. 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

    Article  CAS  Google Scholar 

  30. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  CAS  Google Scholar 

  31. 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, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303

    Article  CAS  Google Scholar 

  32. Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35:D169-172. https://doi.org/10.1093/nar/gkl889

    Article  CAS  Google Scholar 

  33. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  Google Scholar 

  34. Kraft Nathan JB, Cornwell William K, Webb Campbell O, Ackerly David D (2007) Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170:271–283. https://doi.org/10.1086/519400

    Article  CAS  Google Scholar 

  35. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448

    Article  Google Scholar 

  36. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  Google Scholar 

  37. Xia S, Shi Y, Fu Y, Ma X (2005) DGGE analysis of 16S rDNA of ammonia-oxidizing bacteria in chemical–biological flocculation and chemical coagulation systems. Appl Microbiol Biotechnol 69:99–105. https://doi.org/10.1007/s00253-005-0035-5

    Article  CAS  Google Scholar 

  38. Hirayama H, Takai K, Inagaki F, Nealson KH, Horikoshi K (2005) Thiobacter subterraneus gen. nov., sp. nov., an obligately chemolithoautotrophic, thermophilic, sulfur-oxidizing bacterium from a subsurface hot aquifer. Int J Syst Evol Microbiol 55:467–472. https://doi.org/10.1099/ijs.0.63389-0

    Article  CAS  Google Scholar 

  39. Swab RM, Lorenz N, Byrd S, Dick R (2017) Native vegetation in reclamation: improving habitat and ecosystem function through using prairie species in mine land reclamation. Ecol Eng 108:525–536. https://doi.org/10.1016/j.ecoleng.2017.05.012

    Article  Google Scholar 

  40. Sheoran V, Sheoran AS, Poonia P (2010) Soil reclamation of abandoned mine land by revegetation: a review. Int J Soil Sediment Water 3:13

    Google Scholar 

  41. Li Y, Wen H, Chen L, Yin T (2014) Succession of bacterial community structure and diversity in soil along a chronosequence of reclamation and re-vegetation on coal mine spoils in china. PLoS ONE 9:e115024. https://doi.org/10.1371/journal.pone.0115024

  42. Wu S-H, Huang B-H, Gao J, Wang S, Liao P-C (2019) The effects of afforestation on soil bacterial communities in temperate grassland are modulated by soil chemical properties. PeerJ 7:e6147. https://doi.org/10.7717/peerj.6147

  43. Wu S-H, Huang B-H, Huang C-L, Li G, Liao P-C (2018) The aboveground vegetation type and underground soil property mediate the divergence of soil microbiomes and the biological interactions. Microb Ecol 75:434–446. https://doi.org/10.1007/s00248-017-1050-7

    Article  CAS  Google Scholar 

  44. Šnajdr J, Dobiášová P, Urbanová M, Petránková M, Cajthaml T, Frouz J, Baldrian P (2013) Dominant trees affect microbial community composition and activity in post-mining afforested soils. Soil Biol Biochem 56:105–115. https://doi.org/10.1016/j.soilbio.2012.05.004

    Article  CAS  Google Scholar 

  45. Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, Den Haag, the Netherlands

  46. Ravenek JM, Mommer L, Visser EJW, van Ruijven J, van der Paauw JW, Smit-Tiekstra A, de Caluwe H, de Kroon H (2016) Linking root traits and competitive success in grassland species. Plant Soil 407:39–53. https://doi.org/10.1007/s11104-016-2843-z

    Article  CAS  Google Scholar 

  47. Tjoelker MG, Craine JM, Wedin D, Reich PB, Tilman D (2005) Linking leaf and root trait syndromes among 39 grassland and savannah species. New Phytol 167:493–508. https://doi.org/10.1111/j.1469-8137.2005.01428.x

    Article  CAS  Google Scholar 

  48. Heinen R, Hannula SE, De Long JR, Huberty M, Jongen R, Kielak A, Steinauer K, Zhu F, Bezemer TM (2020) Plant community composition steers grassland vegetation via soil legacy effects. Ecol Lett 23:973–982. https://doi.org/10.1111/ele.13497

    Article  Google Scholar 

  49. Hannula SE, Kielak AM, Steinauer K, Huberty M, Jongen R, De Long JR, Heinen R, Bezemer TM (2019) Time after time: temporal variation in the effects of grass and forb species on soil bacterial and fungal communities. mBio 10:e02635-02619. https://doi.org/10.1128/mBio.02635-19

    Article  Google Scholar 

  50. Vieira S, Sikorski J, Dietz S, Herz K, Schrumpf M, Bruelheide H, Scheel D, Friedrich MW, Overmann J (2020) Drivers of the composition of active rhizosphere bacterial communities in temperate grasslands. ISME J 14:463–475. https://doi.org/10.1038/s41396-019-0543-4

    Article  CAS  Google Scholar 

  51. Violle C, Nemergut DR, Pu Z, Jiang L (2011) Phylogenetic limiting similarity and competitive exclusion. Ecol Lett 14:782–787. https://doi.org/10.1111/j.1461-0248.2011.01644.x

    Article  Google Scholar 

  52. Gerhold P, Cahill JF Jr, Winter M, Bartish IV, Prinzing A (2015) Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). Funct Ecol 29:600–614. https://doi.org/10.1111/1365-2435.12425

    Article  Google Scholar 

  53. Trivedi C, Reich PB, Maestre FT, Hu H-W, Singh BK, Delgado-Baquerizo M (2019) Plant-driven niche differentiation of ammonia-oxidizing bacteria and archaea in global drylands. ISME J 13:2727–2736. https://doi.org/10.1038/s41396-019-0465-1

    Article  CAS  Google Scholar 

  54. Dastogeer KMG, Tumpa FH, Sultana A, Akter MA, Chakraborty A (2020) Plant microbiome–an account of the factors that shape community composition and diversity. Curr Plant Biol 23:100161. https://doi.org/10.1016/j.cpb.2020.100161

Download references

Acknowledgements

The authors acknowledge the help of Yuan Liu and Biomarker Technologies Corporation (China) with the PacBio sequencing. We also appreciate the assistance of Prof. Gary Bentley with English editing.

Funding

This research was financially supported by the National Natural Science Foundation of China (NSFC31760120) to RHG and by the Ministry of Science and Technology, Taiwan (MOST 109–2621-B-003–003-MY3 and 109–2628-B-003–001) to PCL. This article was also subsidized by the National Taiwan Normal University (NTNU).

Author information

Authors and Affiliations

Authors

Contributions

YZY, RHG, and PCL conceived and designed the experiments. YZY and HXY collected plant materials. YZY and HXY performed the laboratory experiments. MXL, JTC, CTC, and PCL analyzed the data. MXL and PCL wrote the paper. All authors participated in the discussion, critically reviewed the manuscript, and approved the final manuscript.

Corresponding authors

Correspondence to Run-Hong Gao or Pei-Chun Liao.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Conflict of Interest

The authors declare no competing interests.

Additional information

Yong-Zhi Yang, Min-Xin Luo, and Hai-Xia Yan contributed equally to this study.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1192 KB)

Supplementary file2 (CSV 6 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, YZ., Luo, MX., Yan, HX. et al. Physicochemical and Biotic Changes and the Phylogenetic Evenness of Microbial Community in Soil Subjected to Phytoreclamation. Microb Ecol 84, 1182–1194 (2022). https://doi.org/10.1007/s00248-021-01890-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-021-01890-w

Keywords

Navigation