Advertisement

Mycorrhiza

, Volume 26, Issue 6, pp 575–585 | Cite as

Organic amendments increase phylogenetic diversity of arbuscular mycorrhizal fungi in acid soil contaminated by trace elements

  • María del Mar Montiel-Rozas
  • Álvaro López-García
  • Rasmus Kjøller
  • Engracia Madejón
  • Søren Rosendahl
Original Article

Abstract

In 1998, a toxic mine spill polluted a 55-km2 area in a basin southward to Doñana National Park (Spain). Subsequent attempts to restore those trace element-contaminated soils have involved physical, chemical, or biological methodologies. In this study, the restoration approach included application of different types and doses of organic amendments: biosolid compost (BC) and leonardite (LEO). Twelve years after the last addition, molecular analyses of arbuscular mycorrhizal (AM) fungal communities associated with target plants (Lamarckia aurea and Chrysanthemum coronarium) as well as analyses of trace element concentrations both in soil and in plants were performed. The results showed an improved soil quality reflected by an increase in soil pH and a decrease in trace element availability as a result of the amendments and dosages. Additionally, the phylogenetic diversity of the AM fungal community increased, reaching the maximum diversity at the highest dose of BC. Trace element concentration was considered the predominant soil factor determining the AM fungal community composition. Thereby, the studied AM fungal community reflects a community adapted to different levels of contamination as a result of the amendments. The study highlights the long-term effect of the amendments in stabilizing the soil system.

Keywords

Trace element contaminated soils Ecosystem restoration Soil biodiversity Mine spill Soil fungal community Bioindicator 

Notes

Acknowledgments

AGL2011-23617 project was supported by the CICYT of the Ministerio de Ciencia e Innovación of Spain and FEDER (EU). M Mar Montiel-Rozas acknowledges support from the Ministerio de Economía y Competitividad (FPI grant, BES-2012-05339).

Supplementary material

572_2016_694_MOESM1_ESM.docx (1024 kb)
Online Resource 1 Distribution of amended plots in the experimental field and location inside of the area affected by mine spill. (DOCX 1023 kb)
572_2016_694_MOESM2_ESM.docx (1 mb)
Online Resource 2 NeighborNet split network on the site dataset based on the Monophyletic Clade Approach. (DOCX 1025 kb)
572_2016_694_MOESM3_ESM.docx (1024 kb)
Online Resource 3 Relative abundance of OTUs identified in each treatment. (DOCX 1023 kb)
572_2016_694_MOESM4_ESM.docx (1 mb)
Online Resource 4 Permutational multivariate analysis of the effect of amendment treatments, plant host identity and spatial processes on arbuscular mycorrhizal community composition. (DOCX 1024 kb)
572_2016_694_MOESM5_ESM.docx (1023 kb)
Online Resource 5 Principal Component Analysis (PCA) of available trace elements in the experimental area. (DOCX 1023 kb)

References

  1. Adriano DC (2001) Trace elements in terrestrial environments. Biogeochemistry, bioavailability, and risks of metals. Springer-Verlag, New YorkCrossRefGoogle Scholar
  2. Adriano DC, Wenzel WW, Vangronsveld J, Bolan NS (2004) Role of assisted natural remediation in environmental cleanup. Geoderma 122:121–142CrossRefGoogle Scholar
  3. Alguacil MM, Diaz-Pereira E, Caravaca F, Fernandez DA, Roldan A (2009) Increased diversity of arbuscular mycorrhizal fungi in a long-term field experiment via application of organic amendments to a semiarid degraded soil. Appl Environ Microbiol 75:4254–4263CrossRefGoogle Scholar
  4. Alguacil MM, Torrecillas E, Caravaca F, Fernández DA, Azcón R, Roldán A (2011) The application of an organic amendment modifies the arbuscular mycorrhizal fungal communities colonizing native seedlings grown in a heavy-metal-polluted soil. Soil Biol Biochem 43:1498–1508CrossRefGoogle Scholar
  5. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693CrossRefPubMedGoogle Scholar
  6. Bedini S, Turrini A, Rigo C, Argese E, Giovannetti M (2010) Molecular characterization and glomalin production of arbuscular mycorrhizal fungi colonizing a heavy metal polluted ash disposal island, downtown Venice. Soil Biol Biochem 42:758–765CrossRefGoogle Scholar
  7. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632CrossRefPubMedGoogle Scholar
  8. Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68CrossRefGoogle Scholar
  9. Burgos P, Madejón E, Pérez de Mora A, Cabrera F (2008) Horizontal and vertical variability of soil properties in a trace element contaminated area. Int J Appl Earth Obs Geoinf 10:11–25CrossRefGoogle Scholar
  10. Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491CrossRefPubMedGoogle Scholar
  11. Chiapello M, Martino E, Perotto S (2015) Common and metal-specific proteomic responses to cadmium and zinc in the metal tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn. Metallomics 7:805–815CrossRefPubMedGoogle Scholar
  12. Costanza JK, Moody A, Peet RK (2011) Multi-scale environmental heterogeneity as a predictor of plant species richness. Landsc Ecol 26:851–864CrossRefGoogle Scholar
  13. Curaqueo G, Schoebitz M, Borie F, Caravaca F, Roldán A (2014) Inoculation with arbuscular mycorrhizal fungi and addition of composted olive-mill waste enhance plant establishment and soil properties in the regeneration of a heavy metal-polluted environment. Environ Sci Pollut Res 21:7403–7412CrossRefGoogle Scholar
  14. de Melo RW, Schneider J, de Souza E, Fonsêca C, Guimarães L, de Souza MF (2014) Phytoprotective effect of arbuscular mycorrhizal fungi species against arsenic toxicity in tropical leguminous species. Int J Phytoremediation 16:840–858CrossRefPubMedGoogle Scholar
  15. Díaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 18:646–655CrossRefGoogle Scholar
  16. Domínguez MT, Alegre JM, Madejón P, Madejón E, Burgos P, Cabrera F, Marañón T, Murillo JM (2016) River banks and channels as hotspots of soil pollution after large-scale remediation of a river basin. Geoderma 261:133–140CrossRefGoogle Scholar
  17. Feddermann N, Finlay R, Boller T, Elfstrand M (2010) Functional diversity in arbuscular mycorrhiza—the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecol 3:1–8CrossRefGoogle Scholar
  18. Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30:581–599CrossRefGoogle Scholar
  19. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530CrossRefPubMedGoogle Scholar
  20. Gollotte A, Van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 14:111–117CrossRefPubMedGoogle Scholar
  21. González-Chávez MC, Carrillo-González R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323CrossRefPubMedGoogle Scholar
  22. González-Guerrero M, Benabdellah K, Ferrol N, Aguilar C (2009) Mechanisms underlying heavy metal tolerance in arbuscular mycorrhizas. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas: functional processes and ecological impact. Springer, Berlin, pp 107–122CrossRefGoogle Scholar
  23. Gosling P, Mead A, Proctor M, Hammond J, Bending G (2013) Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol 198:546–556CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gravel D, Bell T, Barbera C, Combe M, Pommier T, Mouquet N (2012) Phylogenetic constraints on ecosystem functioning. Nat Commun 3:1117–1117CrossRefPubMedGoogle Scholar
  25. Grimalt JO, Ferrer M, Macpherson E (1999) The environmental impact of the mine tailing accident in Aznalcóllar. Sci Total Environ 242:1–337CrossRefGoogle Scholar
  26. Hassan SED, Boon E, St-Arnaud M, Hijri M (2011) Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol Ecol 20:3469–3483CrossRefGoogle Scholar
  27. Hesse PR (1971) A textbook of soil chemical analysis. John Murray, LondonGoogle Scholar
  28. Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146CrossRefPubMedGoogle Scholar
  29. HilleRisLambers J, Adler PB, Harpole WS, Levine JM, Mayfield MM (2012) Rethinking community assembly through the lens of coexistence theory. Annu Rev Ecol Evol Syst 43:227–248CrossRefGoogle Scholar
  30. Horn S, Caruso T, Verbruggen E, Rillig MC, Hempel S (2014) Arbuscular mycorrhizal fungal communities are phylogenetically clustered at small scales. ISME J 8:2231–2242CrossRefPubMedGoogle Scholar
  31. Houba VJG, Temminghoff EJM, Gaikhorst GA, Van Vark W (2000) Soil analysis procedures using 0.01 M calcium chloride as extraction reagent. Commun Soil Sci Plant Anal 31:1299–1396CrossRefGoogle Scholar
  32. Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16Google Scholar
  33. Kaldorf M, Kuhn AJ, Schröder WH, Hildebrandt U, Bothe H (1999) Selective element deposits in maize colonized by a heavy metal tolerance conferring arbuscular mycorrhizal fungus. J Plant Physiol 154:718–728CrossRefGoogle Scholar
  34. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464CrossRefPubMedGoogle Scholar
  35. Kidd P, Barceló J, Bernal MP, Navari-Izzo F, Poschenrieder C, Shilev S, Monterroso C (2009) Trace element behaviour at the root–soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259CrossRefGoogle Scholar
  36. Kumpiene J, Lagerkvist A, Maurice C (2008) Stabilization of As, Cr, Cu, Pb and Zn in soil using amendments—a review. Waste Manag 28:215–225CrossRefPubMedGoogle Scholar
  37. Lavorel S, Grigulis K, Lamarque P, Colace MP, Garden D, Girel J, Pellet G, Douzet R (2011) Using plant functional traits to understand the landscape distribution of multiple ecosystem. J Ecol 99:135–147CrossRefGoogle Scholar
  38. Lee JJ, Park RD, Kim YW, Shim JH, Chae DH, Rim YS, Kim KY (2004) Effect of food waste compost on microbial population, soil enzyme activity and lettuce growth. Bioresour Technol 93:21–28CrossRefPubMedGoogle Scholar
  39. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination species data. Oecologia 129:271–280CrossRefGoogle Scholar
  40. Legendre P, Legendre L (1998) Numerical ecology. Elsevier Science, AmsterdamGoogle Scholar
  41. Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105CrossRefGoogle Scholar
  42. Lekberg Y, Gibbons SM, Rosendahl S (2014) Will different OTU delineation methods change interpretation of arbuscular mycorrhizal fungal community patterns? New Phytol 202:1101–1104CrossRefPubMedGoogle Scholar
  43. Lenoir I, Fontaine J, Lounès-Hadj Sahraoui A (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15CrossRefPubMedGoogle Scholar
  44. Liu Y, Johnson NC, Mao L, Shi G, Jiang S, Ma X, Feng H (2015) Phylogenetic structure of arbuscular mycorrhizal community shifts in response to increasing soil fertility. Soil Biol Biochem 89:196–205CrossRefGoogle Scholar
  45. López-García A, Hempel S, Miranda JD, Rillig MC, Barea JM, Azcón-Aguilar C (2013) The influence of environmental degradation processes on the arbuscular mycorrhizal fungal community associated with yew (Taxus baccata L.), an endangered tree species from Mediterranean ecosystems of Southeast Spain. Plant Soil 370:355–366CrossRefGoogle Scholar
  46. Madejón E, Pérez de Mora A, Felipe E, Burgos P, Cabrera F (2006) Soil amendments reduce trace element solubility in a contaminated soil and allow regrowth of natural vegetation. Environ Pollut 139:40–52CrossRefPubMedGoogle Scholar
  47. Madejón E, Madejón P, Burgos P, Pérez de Mora A, Cabrera F (2009) Trace elements, pH and organic matter evolution in contaminated soils under assisted natural remediation: a 4-year field study. J Hazard Mater 162:931–938CrossRefPubMedGoogle Scholar
  48. Maherali H, Klironomos J (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748CrossRefPubMedGoogle Scholar
  49. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  50. Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Env Sci Technol 42:741–775CrossRefGoogle Scholar
  51. Mouillot D, Graham NAJ, Villeger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177CrossRefPubMedGoogle Scholar
  52. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364CrossRefGoogle Scholar
  53. Ohsowski BM, Klironomos JN, Dunfield KE, Hart MM (2012) The potential of soil amendments for restoring severely disturbed grasslands. Appl Soil Ecol 60:77–83CrossRefGoogle Scholar
  54. Oksanen J, Blanchet FG, Kindt R, Legendre R, Minchin PR, O’Hara RB et al. (2012) Vegan: community ecology package, R Package Version 2.1-17 edn.Google Scholar
  55. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. U.S. Department of Agriculture. Report 939.Google Scholar
  56. Park JH, Lamb D, Paneerselvam P, Choppala G, Bolan N, Chung JW (2011) Role of organic amendments on enhanced bioremediation of heavy metal(loid) contaminated soils. J Hazard Mater 185:549–574CrossRefPubMedGoogle Scholar
  57. Pérez de Mora A, Madejón P, Burgos P, Cabrera F, Lepp N, Madejón E (2011) Phytostabilization of semiarid soils residually contaminated with trace elements using by-products: sustainability and risks. Environ Pollut 159:3018–3027CrossRefPubMedGoogle Scholar
  58. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799CrossRefPubMedGoogle Scholar
  59. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc Roy Soc Lond B Biol Sci 276:4237–4245CrossRefGoogle Scholar
  60. Powell JR, Monaghan MT, Öpik M, Rillig MC (2011) Evolutionary criteria outperform operational approaches in producing ecologically relevant fungal species inventories. Mol Ecol 20:655–666CrossRefPubMedGoogle Scholar
  61. 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 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  62. Schneider J, Stürmer S, Guimarães L, de Souza MF, de Sousa Soares CF (2013) Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil. J Hazard Mater 262:1105–1115CrossRefPubMedGoogle Scholar
  63. Stockinger H, Krüger M, Schüßler A (2010) DNA barcoding of arbuscular mycorrhizal fungi. New Phytol 187:461–474CrossRefPubMedGoogle Scholar
  64. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  65. Toljander JF, Santos-González JC, Tehler A, Finlay RD (2008) Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial. FEMS Microbiol Ecol 65:323–338CrossRefPubMedGoogle Scholar
  66. Treseder K, Allen M (2002) Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–515CrossRefGoogle Scholar
  67. Vallino M, Massa N, Lumini E, Bianciotto V, Berta G, Bonfante P (2006) Assessment of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environ Microbiol 8:971–983CrossRefPubMedGoogle Scholar
  68. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 74:69–72Google Scholar
  69. Van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Mol Ecol 7:879–887CrossRefPubMedGoogle Scholar
  70. Vellend M (2010) Conceptual synthesis in community ecology. Q Rev Biol 85:183–206CrossRefPubMedGoogle Scholar
  71. Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–217CrossRefPubMedGoogle Scholar
  72. Wagg C, Bender S, Widmer F, van der Heijden M (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270CrossRefPubMedPubMedCentralGoogle Scholar
  73. Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and a proposed determination of the chromic acid titration method. Soil Sci 37:29–38CrossRefGoogle Scholar
  74. Wang F, Wang L, Shi Z, Li Y, Song Z (2012) Effects of AM inoculation and organic amendment, alone or in combination, on growth, p nutrition, and heavy-metal uptake of tobacco in Pb-Cd-contaminated soil. J Plant Growth Regul 31:549–559CrossRefGoogle Scholar
  75. Wang Y, Zhao X, Wang L, Jin S, Zhu W, Lu Y, Wang S (2016) A five-year P fertilization pot trial for wheat only in a rice-wheat rotation of Chinese paddy soil: interaction of P availability and microorganism. Plant Soil 399:305–318CrossRefGoogle Scholar
  76. Warnock DD, Lehmann J, Kuyper TW, Rillig MC (2007) Mycorrhizal responses to biochar in soil—concepts and mechanisms. Plant Soil 300:9–20CrossRefGoogle Scholar
  77. Webb C, Ackerly D, McPeek M, Donoghue M (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505CrossRefGoogle Scholar
  78. Yang Y, Song Y, Scheller HV, Ghosh A, Ban Y, Chen H, Tang M (2015) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158CrossRefGoogle Scholar
  79. Zarei M, König S, Hempel S, Nekouei MK, Savaghebi GH, Buscot F (2008) Community structure of arbuscular mycorrhizal fungi associated to Veronica rechingeri at the Anguran zinc and lead mining region. Environ Pollut 156:1277–1283CrossRefPubMedGoogle Scholar

Further Reading

  1. Huson DH, Rupp R, Scornavacca C (2011) Phylogenetic networks: concepts, algorithms and applications. Cambridge University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • María del Mar Montiel-Rozas
    • 1
  • Álvaro López-García
    • 2
  • Rasmus Kjøller
    • 2
  • Engracia Madejón
    • 1
  • Søren Rosendahl
    • 2
  1. 1.Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS-CSIC) Avda. Reina MercedesSevillaSpain
  2. 2.Department of BiologyUniversity of CopenhagenCopenhagen ØDenmark

Personalised recommendations