Skip to main content

Arbuscular mycorrhizal fungal diversity in soils underlying moss biocrusts in coal mining subsidence areas

Environmental Science and Pollution Research volume 28, pages 3484–3493 (2021)Cite this article

Abstract

The potentially symbiotic mycorrhizal associations dominated by arbuscular mycorrhizal (AM) fungi have become a new topic in bioremediation research in response to global change. Biological soil crusts (biocrusts) play an important role in arid and semi-arid ecosystems. However, AM fungal diversity in the soils underlying moss biocrusts in coal mining subsidence areas remains poorly understood. Here, samples of the soil underlying moss biocrusts in an area inoculated with an AM fungus (AM-BS) and an uninoculated area (CK-BS) plus soil samples from an uninoculated bare area (CK-NBS) were collected from the subsidence area of Shendong Daliuta mine at Yulin, northwest China. AM fungal community diversity indices were maximum in AM-BS, intermediate in CK-BS, and minimum in CK-NBS (P < 0.05). In addition, redundancy analysis (RDA) indicates that the importance of moss biocrust to soil properties followed the sequence: soil water content (SWC) > glomalin-related soil protein (TG) > available phosphorus (Olsen-P) > soil organic matter (SOM) > easily extractable glomalin-related soil protein (EEG) > pH > available nitrogen (alkali-N). SWC, alkali-N, Olsen-P, and SOM were significantly related to the abundance of Glomus and Claroideoglomus, and TG, EEG, and pH were positively related to Diversisipora. In summary, inoculation with the exotic AM fungus and moss biocrust cover created a eutrophic microhabitat for AM fungi in the soils underlying moss biocrusts in the coal mining subsidence area.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

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

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Bao SD (2000) Agro-chemical analysis of soil. Agricultural Publish House of China, Beijing

    Google Scholar 

  • Barger NN, Weber B, Garcia-Pichel F, Zaady E, Belnap J (2016) Patterns and controls on nitrogen cycling of biological soil crusts. In: Weber B, Büdel B, Belnap J (Eds) Biological Soil Crusts: An Organizing Principle in Drylands. Ecological Studies. Springer International Publishing AG, Switzerland, pp 257–285

  • Belnap J, Büdel B, Lange OL (2003) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (Eds) Biological Soil Crusts: Structure, Function, and Management. Springer-Verlag Berlin Heidelberg, New York, pp 3–30

    Chapter  Google Scholar 

  • Belnap J, Weber B, Büdel B (2016) Biological soil crusts as an organizing principle in drylands. In: Weber B, Büdel B, Belnap J (Eds) Biological Soil Crusts: An Organizing Principle in Drylands. Ecological Studies. Springer International Publishing AG, Switzerland, pp 3–13

    Chapter  Google Scholar 

  • Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol 6:1559

    Article  Google Scholar 

  • Bi YL, Xiao L, Sun JH (2019) An arbuscular mycorrhizal fungus ameliorates plant growth and hormones after moderate root damage due to simulated coal mining subsidence: a microcosm study. Environ Sci Pollut R 26:11053–11061

    CAS  Article  Google Scholar 

  • Bowker MA, Belnap J, Büdel B, Sannier C, Pietrasiak N, Eldridge DJ, Rivera-Aguilar V (2016) Controls on distribution patterns of biological soil crusts at micro-to global scales. In: Weber B, Büdel B, Belnap J (Eds) Biological Soil Crusts: An Organizing Principle in Drylands. Ecological Studies. Springer International Publishing AG, Switzerland, pp 173–197

    Chapter  Google Scholar 

  • Brom J, Nedbal V, Procházka J, Pecharová E (2012) Changes in vegetation cover, moisture properties and surface temperature of a brown coal dump from 1984 to 2009 using satellite data analysis. Ecol Eng 43:45–52

    Article  Google Scholar 

  • Castillo-Monroy AP, Bowker MA, Garcia-Palacios P (2015) Aspects of soil lichen biodiversity and aggregation interact to influence subsurface microbial function. Plant Soil 386:303–316

    CAS  Article  Google Scholar 

  • Cejpek J, Kuráž V, Frouz J (2013) Hydrological properties of soils in reclaimed and unreclaimed sites after brown-coal mining. Pol J Environ Stud 22:645–659

    Google Scholar 

  • Chen C, Zhang JN, Lu M, Qin C, Chen YH, Li Y, Huang QW, Wang JC, Shen ZG, Shen QR (2016) Microbial communities of an arable soil treated for 8 years with organic and inorganic fertilizers. Biol Fertil Soils 52:455–467

    CAS  Article  Google Scholar 

  • Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Pärtel M, Reier Ü, Saks Ü, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973

    CAS  Article  Google Scholar 

  • Ferrenberg S, Faist AM, Howell A, Reed SC (2018) Biocrusts enhance soil fertility and Bromus tectorum growth, and interact with warming to influence germination. Plant Soil 429:77–90

    CAS  Article  Google Scholar 

  • Green TGA, Proctor MCF (2016) Physiology of photosynthetic organisms within biological soil crusts: their adaptation, flexibility, and plasticity. In: Weber B, Büdel B, Belnap J (Eds) Biological Soil Crusts: An Organizing Principle in Drylands. Ecological Studies. Springer International Publishing AG, Switzerland, pp 347–381

  • Guan PT, Zhang XK, Yu J, Cheng YY, Li Q, Andriuzzi WS, Liang WJ (2018) Soil microbial food web channels associated with biological soil crusts in desertification restoration: The carbon flow from microbes to nematodes. Soil Biol Biochem 116:82–90

    CAS  Article  Google Scholar 

  • Hernandez-Hernandez RM, Roldan A, Caravaca F, Rodriguez-Caballero G, Torres MP, Maestre FT, Alguacil MM (2017) Arbuscular mycorrhizal fungal assemblages in biological crusts from a Neotropical savanna are not related to the dominant perennial Trachypogon. Sci Total Environ 575:1203–1210

    CAS  Article  Google Scholar 

  • Hu R, Wang XP, Pan YX, Zhang YF, Zhang H (2014) The response mechanisms of soil N mineralization under biological soil crusts to temperature and moisture in temperate desert regions. Eur J Soil Biol 62:66–73

    CAS  Article  Google Scholar 

  • Janos DP, Garamszegi S, Beltran B (2008) Glomalin extraction and measurement. Soil Biol Biochem 40:728–739

    CAS  Article  Google Scholar 

  • Kuter N, Dilaver Z, Gül E (2014) Determination of suitable plant species for reclamation at an abandoned coal mine area. Int J Min Reclam Environ 28:268–276

    CAS  Article  Google Scholar 

  • Lanfranco L, Bonfante P, Genre A (2016) The mutualistic interaction between plants and arbuscular mycorrhizal fungi. Microbiol Spectr 4:727–747

    Article  Google Scholar 

  • Li XR, Zhang P, Su YG, Jia RL (2012) Carbon fixation by biological soil crusts following revegetation of sand dunes in arid desert regions of China: a four-year field study. Catena 97:119–126

    CAS  Article  Google Scholar 

  • Li XL, Zhu TY, Peng F, Chen Q, Lin S, Christie P, Zhang JL (2015) Inner Mongolian steppe arbuscular mycorrhizal fungal communities respond more strongly to water availability than to nitrogen fertilization. Environ Microbiol 17:3051–3068

    Article  Google Scholar 

  • Ma K, Zhang YX, Ruan MY, Guo J, Chai TY (2019) Land subsidence in a coal mining area reduced soil fertility and led to soil degradation in arid and semi-arid regions. Int J Environ Res Public Health 16:3929

    CAS  Article  Google Scholar 

  • McPherson RA (2007) A review of vegetation-atmosphere interactions and their influences on mesoscale phenomena. Prog Phys Geogr 31:261–285

    Article  Google Scholar 

  • Ping J, Yan S, Gu P, Wu Z, Hu C (2017) Application of MIKE SHE to study the impact of coal mining on river runoff in Gujiao mining area, Shanxi, China. PLoS One 12:e0188949

    Article  Google Scholar 

  • Prasad R, Bhola D, Akdi K, Cruz C, KVSS S, Tuteja N, Varma A (2017) Introduction to Mycorrhiza: Historical Development. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza-Function, Diversity, State of the Art. Springer International Publishing AG, Switzerland pp 2–6

  • Qi JH, Liu YB, Li XR, Zhao LN, Zhang WL, Wang YS (2020) AM fungal diversity analysis of lichen and moss biocrusts in Shapotou Region. Acta Pedologica Sin (Chinese) 57:986–994

    Google Scholar 

  • Qiu L, Bi YL, Jiang B, Wang ZG, Zhang YX, Zhakypbek Y (2019) Arbuscular mycorrhizal fungi ameliorate the chemical properties and enzyme activities of rhizosphere soil in reclaimed mining subsidence in northwestern China. J Arid Land 11:135–147

    Article  Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    CAS  Article  Google Scholar 

  • Rillig MC, Caldwell BA, Wösten HAB, Sollins P (2007) Role of proteins in soil carbon and nitrogen storage: controls on persistence. Biogeochemistry 85:25–44

    CAS  Article  Google Scholar 

  • Sarkar A, Asaeda T, Wang Q, Rashid MH (2015) Arbuscular mycorrhizal influences on growth, nutrient uptake, and use efficiency of Miscanthus sacchariflorus growing on nutrient-deficient river bank soil. Flora 212:46–54

    Article  Google Scholar 

  • Schwarzott D, Walker C, Schussler A (2001) Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomales), is nonmonophyletic. Mol Phylogenet Evol 21:190–197

    CAS  Article  Google Scholar 

  • Smith S E, Read D J (2008) Mycorrhizal Symbiosis. 3rd Edition. Academic Press, New York

    Google Scholar 

  • Van Geel M, Busschaert P, Honnay O, Lievens B (2014) Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. J Microbiol Methods 106:93–100

    Article  Google Scholar 

  • Wang FY (2017) Occurrence of arbuscular mycorrhizal fungi in mining-impacted sites and their contribution to ecological restoration: mechanisms and applications. Crit Rev Environ Sci Technol 47:1901–1957

    Article  Google Scholar 

  • Wang K, He XL, Xie LL, Zhao LL (2018) Arbuscular mycorrhizal fungal community structure and diversity are affected by host plant species and soil depth in the Mu Us Desert, northwest China. Arid Land Res Manag 32:198–211

    Article  Google Scholar 

  • Xiao B, Veste M (2017) Moss-dominated biocrusts increase soil microbial abundance and community diversity and improve soil fertility in semi-arid climates on the Loess Plateau of China. Appl Soil Ecol 117:165–177

    Article  Google Scholar 

  • Xiao B, Hu KL, Ren TS, Li BG (2016) Moss-dominated biological soil crusts significantly influence soil moisture and temperature regimes in semiarid ecosystems. Geoderma 263:35–46

    Article  Google Scholar 

  • Xiao L, Bi YL, Du SZ, Wang Y, Guo C (2019) Effects of re-vegetation type and arbuscular mycorrhizal fungal inoculation on soil enzyme activities and microbial biomass in coal mining subsidence areas of Northern China. Catena 177:202–209

    CAS  Article  Google Scholar 

  • Zhang Y, Guo LD (2007) Arbuscular mycorrhizal structure and fungi associated with mosses. Mycorrhiza 17:319–325

    Article  Google Scholar 

Download references

Acknowledgments

We thank Dr. Peter Christie for a final revision of the manuscript and we also thank the editor and reviewers for their valuable suggestions on an earlier version of the manuscript.

Funding

The National Natural Science Foundation of China (51974326, 51574253) and the Capital Science and Technology Talents Training Project (Beijing) (Z18110006318021) funded this study.

Author information

Affiliations

  1. State Key Laboratory of Coal Resources and Safe Mining, China University of Mining and Technology (Beijing), Beijing, 100083, China

    Yinli Bi, Yun Guo & Huan Sun

  2. College of Geology and Environment, Xi’an University of Science and Technology, Xi’an, 710054, China

    Yinli Bi

Authors
  1. Yinli Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yun Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yinli Bi designed the experiments; Huan Sun carried out the experiments; Yinli Bi and Yun Guo analyzed the experimental data and wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yinli Bi.

Ethics declarations

Ethical approval

Not applicable

Consent to participate

Not applicable

Consent to Publish

Not applicable

Competing interests

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Responsible editor: Diane Purchase

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bi, Y., Guo, Y. & Sun, H. Arbuscular mycorrhizal fungal diversity in soils underlying moss biocrusts in coal mining subsidence areas. Environ Sci Pollut Res 28, 3484–3493 (2021). https://doi.org/10.1007/s11356-020-10726-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-10726-y

Keywords

  • AM fungal diversity
  • Biological soil crusts
  • Coal mining subsidence
  • Underlying soils