Skip to main content

Advertisement

SpringerLink
Log in

Molecular diversity of arbuscular mycorrhizal fungal communities across the gradient of alkaline Fe ore tailings, revegetated waste rock to natural soil sites

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

A Correction to this article was published on 13 February 2020

This article has been updated

Abstract

Arbuscular mycorrhizal (AM) fungi are important to the establishment of native vegetation for mined land rehabilitation, particularly in semi-arid and infertile landscapes. However, the information has been scarce about the colonization of AM fungal community in alkaline magnetite Fe ore tailing sites (without toxic metal (loid) contamination). The present study has characterized the diversity of AM fungi across typical domains of a magnetite Fe ore mine located in 200 km south-east of Geraldton, Western Australia, by adopting high throughput Illumina Miseq sequencing. The investigated domains included two tailing sites without top soil covering (T1 and T2), a rehabilitated area of tailings with top soil covering (R1), a revegetated waste rock area (R2), and two native undisturbed soil sites (S1 and S2). The results indicated that the T1/T2 sites had different AM fungal community structure, compared with R1/R2 and S1/S2 sites. The dominant families were Glomeraceae, Claroideoglomeraceae, Archaeosporaceae, Ambisporaceae, and Paraglomeraceae, with Paraglomeraceae (more than 50%) as the most abundant in the T1/T2 and R1/R2 sites. At genus level, Ambispora spp. and Archaeospora spp. were rich in T1/T2 sites (> 10%), while Glomus spp. were preferably dominant in S1/S2 sites (> 10%). Furthermore, amorphous Fe and available P were found to explain the variations associated with AM fungal community composition, particularly the abundance of Archaeosporaceae and Glomeraceae. The study revealed the AM fungal community composition shift across the gradient of Fe ore mine sites, as well as the effects of revegetation on AM fungal community development. The findings indicate the possible restoration of AM fungal community in the tailings undergoing revegetation, and potential adoption of indigenous AM fungi to rapid phytostabilization of the Fe ore tailings under semi-arid climatic conditions.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

Change history

  • 13 February 2020

    The authors thank the Australian Centre for Ecogenomics in the University of Queensland for conducting Illumina sequencing.

References

  • Alguacil MM, Lozano Z, Campoy MJ, Roldán A (2010) Phosphorus fertilisation management modifies the biodiversity of AM fungi in a tropical savanna forage system. Soil Biol Biochem 42:1114–1122

    CAS  Google Scholar 

  • Ban Y, Xu Z, Zhang H, Chen H, Tang M (2015) Soil chemistry properties, translocation of heavy metals, and mycorrhizal fungi associated with six plant species growing on lead-zinc mine tailings. Ann Microbiol 65:503–515

    CAS  Google Scholar 

  • Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular mycorrhizal fungi in a mown grassland. J Ecol:71–82

  • Bisutti I, Hilke I, Raessler M (2004) Determination of total organic carbon–an overview of current methods. TrAC Trends Anal Chem 23:716–726

    CAS  Google Scholar 

  • Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220(4):1108–1115

    Google Scholar 

  • Bukhari MJ (2002) Arbuscular mycorrhizal (AM) fungal diversity of degraded iron ore mine wastelands of Goa. Goa University

  • Cao J, Feng Y, Lin X, Wang J, Xie X (2017) Iron oxide magnetic nanoparticles deteriorate the mutual interaction between arbuscular mycorrhizal fungi and plant. J Soils Sediments 17:841–851

    CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña 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 [J]. Nat Methods 7(5):335–336

    CAS  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal 6:1621–1624

    CAS  Google Scholar 

  • Caris C, Hördt W, Hawkins H-J, Römheld V, George E (1998) Studies of iron transport by arbuscular mycorrhizal hyphae from soil to peanut and sorghum plants. Mycorrhiza 8:35–39

    CAS  Google Scholar 

  • Castro JL, Souza MG, Rufini M, Guimarães AA, Rodrigues TL, Moreira FMS (2017) Diversity and efficiency of rhizobia communities from iron mining areas using cowpea as a trap plant. Revista Brasileira de Ciência do Solo:41

  • Chu Q, Wang X, Yang Y, Chen F, Zhang F, Feng G (2013) Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza 23:497–505

    CAS  Google Scholar 

  • Clapp J, Young J, Merryweather J, Fitter A (1995) Diversity of fungal symbionts in arbuscular mycorrhizas from a natural community. New Phytol 130:259–265

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Google Scholar 

  • Cornwell WK, Bedford BL, Chapin CT (2001) Occurrence of arbuscular mycorrhizal fungi in a phosphorus-poor wetland and mycorrhizal response to phosphorus fertilization. Am J Bot 88:1824–1829

    CAS  Google Scholar 

  • Cross AT, Lambers H (2017) Young calcareous soil chronosequences as a model for ecological restoration on alkaline mine tailings. Sci Total Environ 607-608:168–175

    CAS  Google Scholar 

  • De Caceres M, Jansen F. Indicspecies: studying the statistical relationship between species and groups of sites. R package version 16. 7 (14-01-2013)

  • de Mello CMA, da Silva GA, de Assis DMA, de Pontes JS, de Almeida Ferreira AC, Leão MPC, et al. Paraglomus pernambucanum sp. nov. and Paraglomus bolivianum comb. nov., and biogeographic distribution of Paraglomus and Pacispora. J Appl Bot Food Qual 2013; 86

  • De Miranda J, Harris P (1994) Effects of soil phosphorus on spore germination and hyphal growth of arbuscular mycorrhizal fungi. New Phytol 128:103–108

    CAS  Google Scholar 

  • Dolling P, Ritchie G (1985) Estimates of soil solution ionic strength and the determination of pH in West Australian soils. Soil Research 23(2):309–314

    CAS  Google Scholar 

  • Edgar R (2010) Usearch. Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

  • Entry JA, Rygiewicz PT, Watrud LS, Donnelly PK (2002) Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Adv Environ Res 7:123–138

    CAS  Google Scholar 

  • Eom A-H, Hartnett DC, Wilson GW (2000) Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122:435–444

    Google Scholar 

  • Feng Y, Cui X, He S, Dong G, Chen M, Wang J et al (2013) The role of metal nanoparticles in influencing arbuscular mycorrhizal fungi effects on plant growth. Environ Sci Technol 47:9496–9504

    CAS  Google Scholar 

  • Grant C, Bittman S, Montreal M, Plenchette C, Morel C (2005) Soil and fertilizer phosphorus: effects on plant P supply and mycorrhizal development. Can J Plant Sci 85:3–14

    Google Scholar 

  • Huang L, Baumgartl T, Mulligan D (2012) Is rhizosphere remediation sufficient for sustainable revegetation of mine tailings? Ann Bot 110:223–238

    Google Scholar 

  • Huang L, Baumgartl T, Zhou L, Mulligan D The new paradigm for phytostabilising mine wastes–ecologically engineered pedogenesis and functional root zones. Life-of-Mine 2014. AUSIMM 2014:663–674

  • Jalaluddin M, Hajra N, Firoza K, Shahina F (2008) Effect of Glomus callosum, Meloidogyne incognita and soil moisture on growth and yield of sunflower. Pak J Bot 40:391–396

    Google Scholar 

  • Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders I et al (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176

    Google Scholar 

  • Johnson L (2008) Iron and siderophores in fungal–host interactions. Mycol Res 112:170–183

    CAS  Google Scholar 

  • Kabir Z, O'halloran I, Fyles J, Hamel C (1997) Seasonal changes of arbuscular mycorrhizal fungi as affected by tillage practices and fertilization: hyphal density and mycorrhizal root colonization. Plant Soil 192:285–293

    CAS  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis science 2011; 333: 880–882

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92(4):486–488

    Google Scholar 

  • Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31

    CAS  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    CAS  Google Scholar 

  • Legendre PLL (1998) Numerical ecology. Elsevier, Amsterdam, The Netherlands 1

  • Li T, Lin G, Zhang X, Chen Y, Zhang S, Chen B (2014) Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance. Mycorrhiza 24:595–602

    Google Scholar 

  • Lottermoser B (2010) Tailings, mine wastes (pp. 205–241). Berlin, Heidelberg: Springer Berlin Heidelberg

  • Lugo MA, González Maza ME, Cabello MN (2003) Arbuscular mycorrhizal fungi in a mountain grassland II: seasonal variation of colonization studied, along with its relation to grazing and metabolic host type. Mycologia 95:407–415

    Google Scholar 

  • Lushchak VI (2011) Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 153:175–190

    Google Scholar 

  • Miller R, Jastrow J (2000) Mycorrhizal fungi influence soil structure. Arbuscular mycorrhizas: physiology and function. Springer:3–18

  • Miransari M, Bahrami H, Rejali F, Malakouti M (2009) Effects of soil compaction and arbuscular mycorrhiza on corn (Zea mays L.) nutrient uptake. Soil Tillage Res 103:282–290

    Google Scholar 

  • Morris E, Morris D, Vogt S, Gleber S-C, Bigalke M, Wilcke W, Rillig MC (2019) Visualizing the dynamics of soil aggregation as affected by arbuscular mycorrhizal fungi. The ISME Journal 13:1639–1646

    CAS  Google Scholar 

  • Nogueira M, Nehls U, Hampp R, Poralla K, Cardoso E (2007) Mycorrhiza and soil bacteria influence extractable iron and manganese in soil and uptake by soybean. Plant Soil 298:273–284

    CAS  Google Scholar 

  • Oksanen J (2011) Multivariate analysis of ecological communities in R: vegan tutorial. R package version 1:11–12

    Google Scholar 

  • Olsen SR. Estimation of available phosphorus in soils by extraction with sodium bicarbonate: United States department of agriculture; Washington, 1954

    Google Scholar 

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij J et al (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    Google Scholar 

  • Pawlowska TE, Chaney RL, Chin M, Charvat I (2000) Effects of metal phytoextraction practices on the indigenous community of arbuscular mycorrhizal fungi at a metal-contaminated landfill. Appl Environ Microbiol 66:2526–2530

    CAS  Google Scholar 

  • Phillips JM, Hayman D (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–IN18

    Google Scholar 

  • Porcel R, Aroca R, Ruiz-Lozano JM (2012) Salinity stress alleviation using arbuscular mycorrhizal fungi. A review Agronomy for Sustainable Development 32:181–200

    CAS  Google Scholar 

  • Rayment GE, Lyons DJ. Soil chemical methods: Australasia. Vol 3: CSIRO publishing, 2011

  • Redecker D, Hijri I, Wiemken A (2003) Molecular identification of arbuscular mycorrhizal fungi in roots: perspectives and problems. Folia Geobotanica 38:113–124

    Google Scholar 

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

    CAS  Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363

    Google Scholar 

  • Rodriguez-Echeverria S, Teixeira H, Correia M, Timoteo S, Heleno R, Opik M et al (2017) Arbuscular mycorrhizal fungi communities from tropical Africa reveal strong ecological structure. New Phytol 213:380–390

    Google Scholar 

  • Sánchez-Castro I, Gianinazzi-Pearson V, Cleyet-Marel JC, Baudoin E, Van Tuinen D (2017) Glomeromycota communities survive extreme levels of metal toxicity in an orphan mining site. Sci Total Environ 598:121–128

    Google Scholar 

  • Sato K, Suyama Y, Saito M, Sugawara K (2005) A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl Sci 51:179–181

    CAS  Google Scholar 

  • Schneider J, Stürmer SL, Guilherme LRG, de Souza Moreira FM, Soares CRFS (2013) Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil. J Hazard Mater 262:1105–1115

    CAS  Google Scholar 

  • Sieverding E (1988) Two new species of vesicular arbuscular mycorrhizal fungi in the Endogonaceae from tropical highlands of Africa. Angewandte Botanik (Germany, FR

    Google Scholar 

  • Smith SE, Read DJ (2010) Mycorrhizal symbiosis: Academic press

  • Spruyt A, Buck MT, Mia A, Straker CJ (2014) Arbuscular mycorrhiza (AM) status of rehabilitation plants of mine wastes in South Africa and determination of AM fungal diversity by analysis of the small subunit rRNA gene sequences. S Afr J Bot 94:231–237

    CAS  Google Scholar 

  • Sun Y, Zhang X, Wu Z, Hu Y, Wu S, Chen B (2016) The molecular diversity of arbuscular mycorrhizal fungi in the arsenic mining impacted sites in Hunan Province of China. J Environ Sci (China) 39:110–118

    CAS  Google Scholar 

  • Tchabi A, Coyne D, Hountondji F, Lawouin L, Wiemken A, Oehl F (2008) Arbuscular mycorrhizal fungal communities in sub-Saharan Savannas of Benin, West Africa, as affected by agricultural land use intensity and ecological zone. Mycorrhiza 18:181–195

    Google Scholar 

  • Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304

    CAS  Google Scholar 

  • Trouvelot A, Kough J, Gianinazzi-Pearson V (1986) Evaluation of VA infection levels in root systems. Research for estimation methods having a functional significance. Physiological and genetical aspects of Mycorrhizae:217–221

  • Verma P, Verma R (2017) Species diversity of arbuscular mycorrhizal (AM) fungi in Dalli-Rajhara iron mine overburden dump of Chhattisgarh (Central India). Int J Curr Microbiol App Sci 6:2766–2781

    Google Scholar 

  • Vieira CK, Marascalchi MN, Rodrigues AV, de Armas RD, Stürmer SL (2018) Morphological and molecular diversity of arbuscular mycorrhizal fungi in revegetated iron-mining site has the same magnitude of adjacent pristine ecosystems. J Environ Sci 67:330–343

    Google Scholar 

  • Weissenhorn I, Glashoff A, Leyval C, Berthelin J (1994) Differential tolerance to Cd and Zn of arbuscular mycorrhizal (am) fungal spores isolated from heavy metal-polluted and unpolluted soils. Plant Soil 167:189–196

    CAS  Google Scholar 

  • Wu S, Liu Y, Southam G, Robertson L, Chiu TH, Cross AT, Dixon KW, Stevens JC, Zhong H, Chan TS, Lu YJ, Huang L (2019a) Geochemical and mineralogical constraints in iron ore tailings limit soil formation for direct phytostabilization. Sci Total Environ 651:192–202

  • Wu S, Nguyen TAH, Liu Y, Southam G, Wang S, Chan T-S et al (2019b) Deficiencies of secondary Fe (oxy) hydroxides associated with phyllosilicates and organic carbon limit the formation of water-stable aggregates in Fe-ore tailings. Chem Geol 523:73–87

    CAS  Google Scholar 

  • Wu S, Vosátka M, Vogel-Mikus K, Kavčič A, Kelemen M, Šepec L et al (2018) Nano zero-valent iron mediated metal (loid) uptake and translocation by Arbuscular mycorrhizal symbioses. Environ Sci Technol 52:7640–7651

    CAS  Google Scholar 

  • Wu S, Zhang X, Huang L, Chen B (2019c) Arbuscular mycorrhiza and plant chromium tolerance. Soil Ecol Letters 1(3–4):94–104

    Google Scholar 

  • Wu S, Liu Y, Bougoure JJ, Southam G, Chan TS, Lu YR, Haw SC, Nguyen TA, You F, Huang LH (2019d) Organic matter amendment and plant colonization drive mineral weathering, organic carbon sequestration and water stable aggregation in magnetite Fe ore tailings. Environ Sci Technol 53(23):13720–13731

    CAS  Google Scholar 

  • Xiang D, Verbruggen E, Hu Y, Veresoglou SD, Rillig MC, Zhou W et al (2014) Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytol 204:968–978

    CAS  Google Scholar 

  • Yoshimura Y, Ido A, Iwase K, Matsumoto T, Yamato M (2012) Communities of arbuscular mycorrhizal fungi in the roots of Pyrus pyrifolia var. culta (Japanese Pear) in orchards with variable amounts of soil-available phosphorus. Microbes Environ : ME12118

  • Yuan M, Xu ZP, Baumgartl T, Huang L (2016) Organic amendment and plant growth improved aggregation in Cu/Pb-Zn tailings. Soil Sci Soc Am J 80:27–37

    CAS  Google Scholar 

  • Zarei M, Saleh-Rastin N, Jouzani GS, Savaghebi G, Buscot F (2008) Arbuscular mycorrhizal abundance in contaminated soils around a zinc and lead deposit. Eur J Soil Biol 44:381–391

    CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Australian Centre for Ecogenomics in the University of Queensland for conducting Illumina sequencing. The authors also acknowledge the financial support from Australia Research Council (ARC) Linkage project (ARC-LP 019806) (Australian Research Council, Kara Mining Ltd., Botanic Gardens & Parks Authority) and UQ ECR funding (613767).

Author information

Author notes

  1. Songlin Wu and Fang You contributed equally to this work.

Authors and Affiliations

  1. Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, Brisbane, Queensland, 4072, Australia

    Songlin Wu, Fang You, Merinda Hall & Longbin Huang

  2. Jiangxi Engineering and Technology Research Center for Ecological Remediation of Heavy Metal Pollution, Institute of Biological Resources, Jiangxi Academy of Sciences, Nanchang, 330096, China

    Zhaoxiang Wu

  3. Advanced Water Management Centre, The University of Queensland, Brisbane, Queensland, 4072, Australia

    Philip Bond

Authors
  1. Songlin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fang You
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhaoxiang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philip Bond
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Merinda Hall
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Longbin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Longbin Huang.

Additional information

Responsible Editor: Diane Purchase

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 6142 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, S., You, F., Wu, Z. et al. Molecular diversity of arbuscular mycorrhizal fungal communities across the gradient of alkaline Fe ore tailings, revegetated waste rock to natural soil sites. Environ Sci Pollut Res 27, 11968–11979 (2020). https://doi.org/10.1007/s11356-020-07780-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-07780-x

Keywords

Search

Navigation