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.
Similar content being viewed by others
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344
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
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
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
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
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
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. doi:10.1093/molbev/msj030
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
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
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
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
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
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination species data. Oecologia 129:271–280. doi:10.1007/s004420100716
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
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
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
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
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
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
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
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
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
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
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
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
Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39. doi:10.1146/annurev.arplant.56.032604.144214
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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).”
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(DOCX 298 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-017-1181-5