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Native soil organic matter as a decisive factor to determine the arbuscular mycorrhizal fungal community structure in contaminated soils

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Abstract

The present study of arbuscular mycorrhizal (AM) fungi is focused on the identification of AM ecotypes associated with different plants species (Poa annua, Medicago polymorpha, and Malva sylvestris) growing in three contaminated soils with different organic matter, phosphorus, and trace element (TE; Cu, Cd, Mn, and Zn) contents. Soils were amended with biosolid and alperujo compost. Shifts in AM fungal community structure, diversity, richness, root colonization, and plant TE uptake were evaluated. Soil properties and plant species had a significant effect on AM fungal community composition as well as on root colonization. However, AM fungal diversity and richness were only affected by soil properties and especially by soil organic matter that was a major driver of AM fungal community. As soil quality increased, Glomeraceae decreased in favor of Claroideoglomeraceae in the community, AM fungal diversity and richness increased, and root colonization decreased. No effect due to amendment (exogenous organic matter) addition was found either in AM fungal parameters measured or TE plant uptake. Our results revealed that the role of TE contamination was secondary for the fungal community behavior, being the native organic matter content the most significant factor.

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References

  • Affholder MC, Pricop AD, Laffont-Schwob I, Coulomb B, Rabier J, Borla A, Prudent P (2014) As, Pb, Sb, and Zn transfer from soil to root of wild rosemary: do native symbionts matter? Plant Soil 382:219–236. doi:10.1007/s11104-014-2135-4

    Article  CAS  Google Scholar 

  • Carrasco L, Caravaca F, Álvarez-Rogel J, Roldán A (2006) Microbial processes in the rhizosphere soil of a heavy metals-contaminated Mediterranean salt marsh: a facilitating role of AM fungi. Chemosphere 64:104–111. doi:10.1016/j.chemosphere.2005.11.038

    Article  CAS  PubMed  Google Scholar 

  • Cavagnaro T (2014) Impacts of compost application on the formation and functioning of arbuscular mycorrhizas. Soil Biol Biochem 78:38–44. doi:10.1016/j.soilbio.2014.07.007

    Article  CAS  Google Scholar 

  • Chagnon PL, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491. doi:10.1016/j.tplants.2013.05.001

    Article  CAS  PubMed  Google Scholar 

  • Christophersen HM, Smith FA, Smith SE (2009) Arbuscular mycorrhizal colonization reduces arsenate uptake in barley via downregulation of transporters in the direct epidermal phosphate uptake pathway. New Phytol 184:962–974. doi:10.1111/j.1469-8137.2009.03009.x

    Article  CAS  PubMed  Google Scholar 

  • Ciadamidaro L, Puschenreiter M, Santner J, Wenzel WW, Madejón P, Madejón E (2015) Assessment of trace element phytoavailability in compost amended soils using different methodologies. J Soils Sediments . doi:10.1007/s11368-015-1283-3in press

    Google Scholar 

  • Clemente R, Pardo T, Madejón P, Madejón E, Bernal MP (2015) Food byproducts as amendments in trace elements contaminated soils. Food Res Int 73:176–189. doi:10.1016/j.foodres.2015.03.040

    Article  CAS  Google Scholar 

  • Cozzolino V, Di Meo V, Monda H, Spaccini R, Piccolo A (2016a) The molecular characteristics of compost affect plant growth, arbuscular mycorrhizal fungi, and soil microbial community composition. Biol Fertil Soils 52:15–29. doi:10.1007/s00374-015-1046-8

    Article  CAS  Google Scholar 

  • Cozzolino V, De Martino A, Nebbioso A, Di Meo V, Salluzzo A, Piccolo A (2016b) Plant tolerance to mercury in a contaminated soil is enhanced by the combined effects of humic matter addition and inoculation with arbuscular mycorrhizal fungi. Environ Sci Pollut R 23:11312–11322. doi:10.1007/s11356-016-6337-6

    Article  CAS  Google Scholar 

  • Duong T, Penfold C, Marschner P (2012) Amending soils of different texture with six compost types: impact on soil nutrient availability, plant growth and nutrient uptake. Plant Soil 354:197–209. doi:10.1007/s11104-011-1056-8

    Article  CAS  Google Scholar 

  • 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 3:1–8. doi:10.1016/j.funeco.2009.07.003

    Article  Google Scholar 

  • Firmin S, Labidi S, Fontaine J, Laruelle F, Tisserant B, Nsanganwimana F, Pourrut B, Dalpé Y, Grandmougin A, Douay F, Shirali P, Verdin A, Lounès-Hadj Sahraoui A (2015) Arbuscular mycorrhizal fungal inoculation protects Miscanthus×giganteus against trace element toxicity in a highly metalcontaminated site. Sci Total Environ 527–528:91–99. doi:10.1016/j.scitotenv.2015.04.116

  • Gaur A, Adholeya A (2004) Prospects of arbuscular mycorrhizal fungi in phytoremediation of heavy metal contaminated soils. Curr Sci India 86:528–534

    CAS  Google Scholar 

  • 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 14:111–117. doi:10.1007/s00572-003-0244-7

    Article  PubMed  Google Scholar 

  • González-Chávez MC, Carrillo-González R, Gutiérrez-Castorena MC (2009) Natural attenuation in a slag heap contaminated with cadmium: the role of plants and arbuscular mycorrhizal fungi. J Hazard Mater 161:1288–1298. doi:10.1016/j.jhazmat.2008.04.110

    Article  PubMed  Google Scholar 

  • 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 107–122

    Chapter  Google Scholar 

  • Grimalt JO, Ferrer M, MacPherson E (1999) The mine tailing accident in Aznalcóllar. Sci Total Environ 242:3–11. doi:10.1016/S0048-9697(99)00372-1

    Article  CAS  PubMed  Google Scholar 

  • Gryndler M, Hršelová H, Sudová R, Gryndlerová H, Řezáčová V, Merhautová V (2005) Hyphal growth and mycorrhiza formation by the arbuscular mycorrhizal fungus Glomus claroideum BEG 23 is stimulated by humic substances. Mycorrhiza 15:483–488. doi:10.1007/s00572-005-0352-7

    Article  CAS  PubMed  Google Scholar 

  • Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344

    Article  Google Scholar 

  • Hassan SED, Boon E, St-Arnaud M, Hijri M (2011) Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Mol Ecol 20:3469–3483. doi:10.1111/j.1365-294X.2011.05142.x

    Article  Google Scholar 

  • Hassan SED, Hijri M, St-Arnaud M (2013) Effect of arbuscular mycorrhizal fungi on trace metal uptake by sunflower plants grown on cadmium contaminated soil. New Biotechnol 30:780–787. doi:10.1016/j.nbt.2013.07.002

    Article  CAS  Google Scholar 

  • Hazard C, Boots B, Keith AM, Mitchell DT, Schmidt O, Doohan FM, Bending GD (2014) Temporal variation outweighs effects of biosolids applications in shaping arbuscular mycorrhizal fungi communities on plants grown in pasture and arable soils. Appl Soil Ecol 82:52–60. doi:10.1016/j.apsoil.2014.05.007

    Article  Google Scholar 

  • Hernández-Cuevas L, Guadarrama-Chávez P, Sánchez-Gallén I, Ramos-Zapata J (2008) Micorriza arbuscular: colonización intrarradical y extracción de esporas. In: Álvarez-Sánchez J, Monroy-Ata A (eds) Técnicas de Estudio de las Asociaciones Micorrízicas y sus Implicaciones en la Restauración. Facultad de Ciencias. Universidad Nacional Autónoma de México, México D.F, pp 1–15

    Google Scholar 

  • 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 31:1299–1396. doi:10.1080/00103620009370514

    Article  CAS  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. doi:10.1093/molbev/msj030

    Article  CAS  PubMed  Google Scholar 

  • Juniper S, Abbott LK (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379. doi:10.1007/s00572-006-0046-9

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1093/bioinformatics/btq166

    Article  CAS  PubMed  Google Scholar 

  • Kidd P, Barcelo J, Bernal M, Navari-Izzo F, Poschenrieder C, Shilev S, Clemente R, Monterroso C (2009) Trace element behaviour at the root-soil interface: implications in phytoremediation. Environ Exp Bot 67:243–259. doi:10.1016/j.envexpbot.2009.06.013

    Article  CAS  Google Scholar 

  • Klironomos JN, Hart MM (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza 12:181–184. doi:10.1007/s00572-002-0169-6

    Article  PubMed  Google Scholar 

  • Krishnamoorthy R, Kim CG, Subramanian P, Kim KY, Selvakumar G, Sa TM (2015) Arbuscular mycorrhizal fungi community structure, abundance and species richness changes in soil by different levels of heavy metal and metalloid concentration. PLoS One 10:e0128784. doi:10.1371/journal.pone.0128784

    Article  PubMed  PubMed Central  Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination species data. Oecologia 129:271–280. doi:10.1007/s004420100716

    Article  Google Scholar 

  • 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 95:95–105. doi:10.1111/j.1365-2745.2006.01193.x

    Article  Google Scholar 

  • Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. The ISME Journal 7:1424–1433. doi:10.1038/ismej.2013.41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lekberg Y, Gibbons SM, Rosendahl S (2014) Will different OTU delineation methods change interpretation of arbuscular mycorrhizal fungal community patterns? New Phytol 202:1101–1104. doi:10.1111/nph.12758

    Article  PubMed  Google Scholar 

  • Lenoir I, Fontaine J, Lounès-Hadj Sahraoui A (2016) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15. doi:10.1016/j.phytochem.2016.01.002

    Article  CAS  PubMed  Google Scholar 

  • Marques APGC, Oliveira RS, Rangel AOSS, Castro PML (2006) Zinc accumulation in Solanum nigrum is enhanced by different arbuscular mycorrhizal fungi. Chemosphere 65:1256–1263. doi:10.1016/j.chemosphere.2006.03.022

    Article  CAS  PubMed  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297. doi:10.2307/2680104

    Article  Google Scholar 

  • Montiel-Rozas MM, Madejón E, Madejón P (2015) Evaluation of phytostabilizer ability of three ruderal plants in mining soils restored by application of organic amendments. Ecol Eng 83:431–436. doi:10.1016/j.ecoleng.2015.04.096

    Article  Google Scholar 

  • Montiel-Rozas MM, López-García Á, Kjøller R, Madejón E, Rosendahl S (2016a) Organic amendments increase phylogenetic diversity of arbuscular mycorrhizal fungi in acid soil contaminated by trace elements. Mycorrhiza 26:575–585. doi:10.1007/s00572-016-0694-3

    Article  CAS  Google Scholar 

  • Montiel-Rozas MM, Madejón E, Madejón P (2016b) Effect of heavy metals and organic matter on root exudates (low molecular weight organic acids) of herbaceous species: an assessment in sand and soil conditions under different levels of contamination. Environ Pollut 216:273–281. doi:10.1016/j.envpol.2016.05.080

    Article  CAS  PubMed  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A, Ma P (2003) Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl Environ Microb 69:2816–2824. doi:10.1128/AEM.69.5.2816

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Wagner H (2012) Vegan: community ecology package, R Package version 2.1-17 edn

  • 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

  • Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790. doi:10.1111/j.1365-2745.2006.01136.x

    Article  Google Scholar 

  • Panagos P, Van Liedekerke M, Yigini Y, Montanarella L (2013) Contaminated sites in Europe: review of the current situation based on data collected through a European network. J Environ Public Health . doi:10.1155/2013/158764ID 158764

    PubMed  PubMed Central  Google Scholar 

  • Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. doi:10.1146/annurev.arplant.56.032604.144214

    Article  CAS  PubMed  Google Scholar 

  • Punamiya P, Datta R, Sarkar D, Barber S, Patel M, Das P (2010) Symbiotic role of Glomus mosseae in phytoextraction of lead in vetiver grass [Chrysopogon zizanioides (L.)]. J Hazard Mater 177:465–474. doi:10.1016/j.jhazmat.2009.12.056

    Article  CAS  PubMed  Google Scholar 

  • Qin H, Lu K, Strong PJ, Xu Q, Wu Q, Xu Z, Wang H (2015) Long-term fertilizer application effects on the soil, root arbuscular mycorrhizal fungi and community composition in rotation agriculture. Appl Soil Ecol 89:35–43. doi:10.1016/j.apsoil.2015.01.008

    Article  Google Scholar 

  • 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 Microb 75:7537–7541. doi:10.1128/AEM.01541-09

    Article  CAS  Google Scholar 

  • Schloter M, Dilly O, Munch JC (2003) Indicators for evaluating soil quality. Agric Ecosyst Environ 98:255–262. doi:10.1016/S0167-8809(03)00085-9

    Article  Google Scholar 

  • Schneider J, Luiz S, Roberto L, Guilherme G (2013) Arbuscular mycorrhizal fungi in arsenic-contaminated areas in Brazil. J Hazard Mater 262:1105–1115. doi:10.1016/j.jhazmat.2012.09.063

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian H, Gai JP, Zhang JL, Christie P, Li XL (2009) Arbuscular mycorrhizal fungi in degraded typical steppe of inner Mongolia. Land Degrad Dev 20:41–54. doi:10.1002/ldr.876

    Article  Google Scholar 

  • Vályi K, Rillig MC, Hempel S (2015) Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. New Phytol 205:1577–1586. doi:10.1111/nph.13236

    Article  PubMed  Google Scholar 

  • Van Der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150. doi:10.1111/j.1365-2745.2009.01570.x

    Article  Google Scholar 

  • Van der Heijden MGA, Scheublin TR (2007) Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174:244–250. doi:10.1111/j.1469-8137.2007.02058.x

    Article  PubMed  Google Scholar 

  • 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 7:879–887. doi:10.1046/j.1365-294x.1998.00410.x

    Article  CAS  PubMed  Google Scholar 

  • Verdin A, Lounès-Hadj Sahraoui A, Fontaine J, Grandmougin-Ferjani A, Durand R (2006) Effects of anthracene on development of an arbuscular mycorrhizal fungus and contribution of the symbiotic association to pollutant dissipation. Mycorrhiza 16:397–405. doi:10.1007/s00572-006-0055-8

    Article  CAS  PubMed  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microb 64:5004–5007

    CAS  Google Scholar 

  • Vogel-Mikuš K, Pongrac P, Kump P, Nečemer M, Regvar M (2006) Colonisation of a Zn, Cd and Pb hyperaccumulator Thlaspi praecox Wulfen with indigenous arbuscular mycorrhizal fungal mixture induces changes in heavy metal and nutrient uptake. Environ Pollut 139:362–371. doi:10.1016/j.envpol.2005.05.005

    Article  PubMed  Google Scholar 

  • Wagg C, Bender SF, Widmer F, van der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270. doi:10.1073/pnas.1320054111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 37:29–38

    Article  CAS  Google Scholar 

  • Wei Y, Hou H, Li J, ShangGuan Y, Xu Y, Zhang J, Wang W (2014) Molecular diversity of arbuscular mycorrhizal fungi associated with an Mn hyperaccumulator—Phytolacca americana, in Mn mining area. Appl Soil Ecol 82:11–17. doi:10.1016/j.apsoil.2014.05.005

    Article  Google Scholar 

  • Winding A, Hund-Rinke K, Rutgers M (2005) The use of microorganisms in ecological soil classification and assessment concepts. Ecotox Environ Safe 62:230–248. doi:10.1016/j.ecoenv.2005.03.026

    Article  CAS  Google Scholar 

  • Yang Y, Song Y, Scheller HV, Ghosh A, Ban Y, Chen H, Tang M (2015a) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158. doi:10.1016/j.soilbio.2015.03.018

    Article  CAS  Google Scholar 

  • Yang Y, Liang Y, Ghosh A, Song Y, Chen H, Tang M (2015b) Assessment of arbuscular mycorrhizal fungi status and heavy metal accumulation characteristics of tree species in a lead-zinc mine area: potential applications for phytoremediation. Environ Sci Pollut R 22:13179–13193. doi:10.1007/s11356-015-4521-8

    Article  CAS  Google Scholar 

  • Zarei M, König S, Hempel S, Khayam Nekouei M, Savaghebi G, Buscot F (2008) Community structure of arbuscular mycorrhizal fungi associated to Veronica rechingeri at the Anguran zinc and lead mining region. Environ Pollut 156:1277–1283. doi:10.1016/j.envpol.2008.03.006

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was made possible by the AGL2014-55717-R project supported by the Spanish Ministry of Economy and Competitiveness the and FEDER (EU). MMar Montiel-Rozas acknowledges support from the MINECO (FPI grant, BES-2012-05339). P. Madejón and E. Madejón are members of the “Unidad Asociada al CSIC de Uso sostenible del suelo y el agua en la agricultura (US-IRNAS).”

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Montiel-Rozas, M.d.M., López-García, Á., Madejón, P. et al. Native soil organic matter as a decisive factor to determine the arbuscular mycorrhizal fungal community structure in contaminated soils. Biol Fertil Soils 53, 327–338 (2017). https://doi.org/10.1007/s00374-017-1181-5

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