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Environmental Metabarcoding Reveals Contrasting Belowground and Aboveground Fungal Communities from Poplar at a Hg Phytomanagement Site

  • Fungal Microbiology
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Abstract

Characterization of microbial communities in stressful conditions at a field level is rather scarce, especially when considering fungal communities from aboveground habitats. We aimed at characterizing fungal communities from different poplar habitats at a Hg-contaminated phytomanagement site by using Illumina-based sequencing, network analysis approach, and direct isolation of Hg-resistant fungal strains. The highest diversity estimated by the Shannon index was found for soil communities, which was negatively affected by soil Hg concentration. Among the significant correlations between soil operational taxonomic units (OTUs) in the co-occurrence network, 80% were negatively correlated revealing dominance of a pattern of mutual exclusion. The fungal communities associated with Populus roots mostly consisted of OTUs from the symbiotic guild, such as members of the Thelephoraceae, thus explaining the lowest diversity found for root communities. Additionally, root communities showed the highest network connectivity index, while rarely detected OTUs from the Glomeromycetes may have a central role in the root network. Unexpectedly high richness and diversity were found for aboveground habitats, compared to the root habitat. The aboveground habitats were dominated by yeasts from the Lalaria, Davidiella, and Bensingtonia genera, not detected in belowground habitats. Leaf and stem habitats were characterized by few dominant OTUs such as those from the Dothideomycete class producing mutual exclusion with other OTUs. Aureobasidium pullulans, one of the dominating OTUs, was further isolated from the leaf habitat, in addition to Nakazawaea populi species, which were found to be Hg resistant. Altogether, these findings will provide an improved point of reference for microbial research on inoculation-based programs of tailings dumps.

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References

  1. van der Heijden MGA, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol. 14:e1002378. doi:10.1371/journal.pbio.1002378

    Article  PubMed  PubMed Central  Google Scholar 

  2. Leff JW, Del Tredici P, Friedman WE, Fierer N (2014) Spatial structuring of bacterial communities within individual Ginkgo biloba trees. Environ. Microbiol. 17:2352–2361. doi:10.1111/1462-2920.12695

    Article  PubMed  Google Scholar 

  3. Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, et al (2015) Biogeography and cultivation affect microbiome composition in the drought-adapted plant subgenus Agave. New Phytol. 209:798–811. doi:10.1111/nph.13697

    Article  PubMed  PubMed Central  Google Scholar 

  4. Balint M, Bartha L, O’Hara RB, et al (2015) Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars. Mol. Ecol. 24:235–248. doi:10.1111/mec.13018

    Article  CAS  PubMed  Google Scholar 

  5. 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 

  6. Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol. 105:1744–1755. doi:10.1111/j.1365-2672.2008.03906.x

    Article  CAS  PubMed  Google Scholar 

  7. Ritpitakphong U, Falquet L, Vimoltust A, et al (2016) The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol. 210:1033–1043. doi:10.1111/nph.13808

    Article  CAS  PubMed  Google Scholar 

  8. Waller F, Achatz B, Baltruschat H, et al (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. U. S. A. 102:13386–13391. doi:10.1073/pnas.0504423102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu. Rev. Entomol. 54:323–342. doi:10.1146/annurev.ento.54.110807.090614

    Article  CAS  PubMed  Google Scholar 

  10. Martínez-Álvarez P, Fernández-González RA, Sanz-Ros AV, et al (2016) Two fungal endophytes reduce the severity of pitch canker disease in Pinus radiata seedlings. Biol. Control 94:1–10. doi:10.1016/j.biocontrol.2015.11.011

    Article  Google Scholar 

  11. Danielsen L, Thürmer A, Meinicke P, et al (2012) Fungal soil communities in a young transgenic poplar plantation form a rich reservoir for fungal root communities. Ecol Evol 2:1935–1948. doi:10.1002/ece3.305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tedersoo L, Bahammad B, Polme S, et al (2014) Global diversity and geography of soil fungi. Science (80- ) 346:1256688

    Article  Google Scholar 

  13. Zappelini C, Karimi B, Foulon J, et al (2015) Diversity and complexity of microbial communities from a chlor-alkali tailings dump. Soil Biol. Biochem. 90:101–110. doi:10.1016/j.soilbio.2015.08.008

    Article  CAS  Google Scholar 

  14. Yergeau E, Lawrence JR, Sanschagrin S, et al (2012) Next-generation sequencing of microbial communities in the Athabasca River and its tributaries in relation to oil sands mining activities. Appl. Environ. Microbiol. 78:7626–7637. doi:10.1128/AEM.02036-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Jumpponen A, Jones KL (2009) Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytol. 184:438–448. doi:10.1111/j.1469-8137.2009.02990.x

    Article  CAS  PubMed  Google Scholar 

  16. Knief C, Delmotte N, Chaffron S, et al (2012) Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J 6:1378–1390. doi:10.1038/ismej.2011.192

    Article  CAS  PubMed  Google Scholar 

  17. Bonito G, Reynolds H, Robeson MS, et al (2014) Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Mol. Ecol. 23:3356–3370. doi:10.1111/mec.12821

    Article  PubMed  Google Scholar 

  18. Foulon J, Zappelini C, Durand A, et al (2016) Impact of poplar-based phytomanagement on soil properties and microbial communities in a metal-contaminated site. FEMS Microbiol. Ecol. 92:fiw163. doi:10.1093/femsec/fiw163

    Article  PubMed  Google Scholar 

  19. Faust K, Sathirapongsasuti JF, Izard J, et al (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Comput. Biol. 8:e1002606. doi:10.1371/journal.pcbi.1002606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Xiang L, Gong S, Yang L, et al (2015) Biocontrol potential of endophytic fungi in medicinal plants from Wuhan Botanical Garden in China. Biol. Control 94:47–55. doi:10.1016/j.biocontrol.2015.12.002

    Article  Google Scholar 

  21. Assad M, Parelle J, Cazaux D, et al (2015) Mercury uptake into poplar leaves. Chem. Aust. 146:1–7. doi:10.1016/j.chemosphere.2015.11.103

    Google Scholar 

  22. Hacquard S, Schadt CW (2015) Towards a holistic understanding of the beneficial interactions across the Populus microbiome. New Phytol. 205:1424–1430. doi:10.1111/nph.13133

    Article  PubMed  Google Scholar 

  23. Maillard F, Girardclos O, Assad M, et al (2016) Dendrochemical assessment of mercury releases from a pond and dredged-sediment landfill impacted by a chlor-alkali plant. Environ. Res. 148:122–126. doi:10.1016/j.envres.2016.03.034

    Article  CAS  PubMed  Google Scholar 

  24. Lefort F, Douglas GC (1999) An efficient micro-method of DNA isolation from mature leaves of four hardwood tree species Acer, Fraxinus, Prunus and Quercus. Ann. For. Sci. 56:259–263. doi:10.1051/forest:19990308

    Article  Google Scholar 

  25. Healey A, Furtado A, Cooper T, Henry RJ (2014) Protocol: a simple method for extracting next-generation sequencing quality genomic DNA from recalcitrant plant species. Plant Methods 10:21. doi:10.1186/1746-4811-10-21

    Article  PubMed  PubMed Central  Google Scholar 

  26. Huang CL, Jian FY, Huang HJ, et al (2014) Deciphering mycorrhizal fungi in cultivated Phalaenopsis microbiome with next-generation sequencing of multiple barcodes. Fungal Divers. 66:77–88. doi:10.1007/s13225-014-0281-x

    Article  Google Scholar 

  27. Smith DP, Peay KG (2014) Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS One 9:e90234. doi:10.1371/journal.pone.0090234

    Article  PubMed  PubMed Central  Google Scholar 

  28. Gweon HS, Oliver A, Taylor J, et al (2015) PIPITS: an automated pipeline for analyses of fungal ITS sequences from the Illumina sequencing platform. Methods Ecol. Evol. 6:973–980. doi:10.1111/2041-210X.12399

    Article  PubMed  PubMed Central  Google Scholar 

  29. Dickie IA (2010) Insidious effects of sequencing errors on perceived diversity in molecular surveys. New Phytol. 188:916–918. doi:10.1111/j.1469-8137.2010.03473.x

    Article  PubMed  Google Scholar 

  30. Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. doi:10.1007/s00572-009-0274-x

    Article  PubMed  Google Scholar 

  31. Kõljalg U, Nilsson RH, Abarenkov K, et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22:5271–5277. doi:10.1111/mec.12481

    Article  PubMed  Google Scholar 

  32. Schloss PD, Westcott SL, Ryabin T, et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541. doi:10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Bell TH, El-Din Hassan S, Lauron-Moreau A, et al (2014) Linkage between bacterial and fungal rhizosphere communities in hydrocarbon-contaminated soils is related to plant phylogeny. ISME J 8:331–343. doi:10.1038/ismej.2013.149

    Article  CAS  PubMed  Google Scholar 

  34. Weiss S, Van Treuren W, Lozupone C, et al (2016) Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J. doi:10.1038/ismej.2015.235

    PubMed  PubMed Central  Google Scholar 

  35. Faust K, Raes J (2012) Microbial interactions: from networks to models. Nat Rev Microbiol 10:538–550. doi:10.1038/nrmicro2832

    Article  CAS  PubMed  Google Scholar 

  36. Christmas R, Avila-Campillo I, Bolouri H, et al (2005) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Am Assoc Cancer Res Educ B 13:2498–2504. doi:10.1101/gr.1239303.metabolite

    Google Scholar 

  37. Faust K, Lima-Mendez G, Lerat JS, et al (2015) Cross-biome comparison of microbial association networks. Front. Microbiol. 6:1–13. doi:10.3389/fmicb.2015.01200

    Article  Google Scholar 

  38. Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front. Microbiol. 5:1–14. doi:10.3389/fmicb.2014.00219

    Article  Google Scholar 

  39. Samczyński Z, Dybczyński RS, Polkowska-Motrenko H, et al (2012) Two new reference materials based on tobacco leaves: certification for over a dozen of toxic and essential elements. ScientificWorldJournal 2012:216380. doi:10.1100/2012/216380

    PubMed  PubMed Central  Google Scholar 

  40. Fu S-F, Sun P-F, Lu H-Y, et al (2016) Plant growth-promoting traits of yeasts isolated from the phyllosphere and rhizosphere of Drosera spathulata Lab. Fungal Biol 120:433–448. doi:10.1016/j.funbio.2015.12.006

    Article  CAS  PubMed  Google Scholar 

  41. Sun PF, Fang WT, Shin LY, et al (2014) Indole-3-acetic acid-producing yeasts in the phyllosphere of the carnivorous plant. 1–22. doi: 10.1371/journal.pone.0114196

  42. Coince A, Cordier T, Lengellé J, et al (2014) Leaf and root-associated fungal assemblages do not follow similar elevational diversity patterns. PLoS One 9:e100668. doi:10.1371/journal.pone.0100668

    Article  PubMed  PubMed Central  Google Scholar 

  43. Nguyen NH, Song Z, Bates ST, et al (2015) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20:241–248. doi:10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  44. Inacio J, Portugal L, Spencer-Martins I, Fonseca A (2005) Phylloplane yeasts from Portugal: seven novel anamorphic species in the Tremellales lineage of the Hymenomycetes (Basidiomycota) producing orange-coloured colonies. FEMS Yeast Res. 5:1167–1183. doi:10.1016/j.femsyr.2005.05.007

    Article  CAS  PubMed  Google Scholar 

  45. Limtong S, Koowadjanakul N (2012) Yeasts from phylloplane and their capability to produce indole-3-acetic acid. World J. Microbiol. Biotechnol. 28:3323–3335. doi:10.1007/s11274-012-1144-9

    Article  CAS  PubMed  Google Scholar 

  46. Barberán A, Bates ST, Casamayor EO, Fierer N (2012) Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–351. doi:10.1038/ismej.2011.119

    Article  PubMed  Google Scholar 

  47. Lupatini M, Suleiman AKA, Jacques RJS, et al (2014) Network topology reveals high connectance levels and few key microbial genera within soils. Front Environ Sci 2:1–11. doi:10.3389/fenvs.2014.00010

    Article  Google Scholar 

  48. Murakami R, Kawakita H, Shirata A (2002) Infection behaviour of conidia of Myrothecium roridum on mulberry leaf and cytological changes of leaf cells infected with the fungus. Séricologia 42:19–38

    Google Scholar 

  49. Shakya M, Gottel N, Castro H, et al (2013) A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS One 8:e76382. doi:10.1371/journal.pone.0076382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Glushakova AM, Chernov IY (2004) Seasonal dynamics in a yeast population on leaves of the common wood sorrel Oxalis acetosella L. Microbiology 73:184–188. doi:10.1023/B:MICI.0000023987.40253.2d

    Article  CAS  Google Scholar 

  51. Jumpponen A, Jones KL (2010) Seasonally dynamic fungal communities in the Quercus macrocarpa phyllosphere differ between urban and nonurban environments. New Phytol. 186:496–513. doi:10.1111/j.1469-8137.2010.03197.x

    Article  CAS  PubMed  Google Scholar 

  52. Balint M, Tiffin P, Hallstrom B, et al (2013) Host genotype shapes the foliar fungal microbiome of balsam poplar (Populus balsamifera). PLoS One 8:e53987. doi:10.1371/journal.pone.0053987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Foulon J, Zappelini C, Durand A, et al (2016) Environmental metabarcoding reveals contrasting microbial communities at two poplar phytomanagement sites. Sci. Total Environ. 571:1230–1240. doi:10.1016/j.scitotenv.2016.07.151

    Article  CAS  PubMed  Google Scholar 

  54. Gottel NR, Castro HF, Kerley M, et al (2011) Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl. Environ. Microbiol. 77:5934–5944. doi:10.1128/AEM.05255-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Regvar M, Likar M, Piltaver A, et al (2010) Fungal community structure under goat willows (Salix caprea L.) growing at metal polluted site: the potential of screening in a model phytostabilisation study. Plant Soil 330:345–356. doi:10.1007/s11104-009-0207-7

    Article  CAS  Google Scholar 

  56. Krpata D, Peintner U, Langer I, et al (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol. Res. 112:1069–1079. doi:10.1016/j.mycres.2008.02.004

    Article  PubMed  Google Scholar 

  57. Hrynkiewicz K, Haug I, Baum C (2008) Ectomycorrhizal community structure under willows at former ore mining sites. Eur. J. Soil Biol. 44:37–44. doi:10.1016/j.ejsobi.2007.10.004

    Article  Google Scholar 

  58. Hrynkiewicz K, Dabrowska G, Baum C, et al (2012) Interactive and single effects of ectomycorrhiza formation and Bacillus cereus on metallothionein MT1 expression and phytoextraction of Cd and Zn by willows. Water Air Soil Pollut. 223:957–968. doi:10.1007/s11270-011-0915-5

    Article  CAS  PubMed  Google Scholar 

  59. Inácio J, Rodrigues MG, Sobral P, Fonseca Á (2004) Characterisation and classification of phylloplane yeasts from Portugal related to the genus Taphrina and description of five novel Lalaria species. FEMS Yeast Res. 4:541–555. doi:10.1016/S1567-1356(03)00226-5

    Article  PubMed  Google Scholar 

  60. Cordier T, Stan, Robin C, et al (2012) The composition of phyllosphere fungal assemblages of European beech (Fagus sylvatica ) varies significantly along an elevation gradient. New Phytol. 196:510–519

    Article  PubMed  Google Scholar 

  61. Jakuschkin B, Fievet V, Schwaller L, et al (2016) Deciphering the pathobiome: intra- and interkingdom interactions involving the pathogen Erysiphe alphitoides. Environ Microbiol 1–11. doi: 10.1007/s00248-016-0777-x

  62. Müller A (2001) The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol. Ecol. 36:11–19

  63. Jean-Philippe SR, Franklin JA, Buckley DS, Hughes K (2011) The effect of mercury on trees and their mycorrhizal fungi. Environ. Pollut. 159:2733–2739. doi:10.1016/j.envpol.2011.05.017

    Article  CAS  PubMed  Google Scholar 

  64. Moller AK, Barkay T, Hansen MA, et al (2014) Mercuric reductase genes (merA) and mercury resistance plasmids in high Arctic snow, freshwater and sea-ice brine. FEMS Microbiol. Ecol. 87:52–63. doi:10.1111/1574-6941.12189

    Article  CAS  PubMed  Google Scholar 

  65. Andrews JH, Harris RF (2000) The ecology and biogeography of microorganisms on plant surfaces

  66. Gadd Geoffrey M, Mowll JL (1985) Copper uptake by yeast-like cells, hyphae and chlamydospores of Aureobasidium pullulans. Exp Mycrobiology 9:230–240

    Google Scholar 

  67. Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol. Res. 111:3–49. doi:10.1016/j.mycres.2006.12.001

    Article  CAS  PubMed  Google Scholar 

  68. Kurtzman CP, Robnett CJ (2014) Description of Kuraishia piskuri f.a., sp. nov., a new methanol assimilating yeast and transfer of phylogenetically related Candida species to the genera Kuraishia and Nakazawaea as new combinations. FEMS Yeast Res. 14:1028–1036. doi:10.1111/1567-1364.12192

    CAS  PubMed  Google Scholar 

  69. Hagler AN, Mendonca-Hagler LC, Phaff HJ (1989) Candida populi, a new species of yeast occurring in exudates of Populus and Betula species. Int. J. Syst. Evol. Microbiol. 39:97–99. doi:10.1099/00207713-39-2-97

    Google Scholar 

  70. Lu L, Yin S, Liu X, et al (2013) Fungal networks in yield-invigorating and -debilitating soils induced by prolonged potato monoculture. Soil Biol. Biochem. 65:186–194. doi:10.1016/j.soilbio.2013.05.025

    Article  CAS  Google Scholar 

  71. Lozupone C, Faust K, Raes J, et al (2012) Identifying genomic and metabolic features that can underlie early successional and opportunistic lifestyles of human gut symbionts. Genome Res. 22:1974–1984. doi:10.1101/gr.138198.112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol. Evol. 12:139–143. doi:10.1016/S0169-5347(97)01001-X

    Article  CAS  PubMed  Google Scholar 

  73. Selosse MA, Strullu-Derrien C, Martin FM, et al (2015) Plants, fungi and oomycetes: a 400-million year affair that shapes the biosphere. New Phytol. 206:501–506. doi:10.1111/nph.13371

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the French National Research Agency [ANR BIOFILTREE 2010-INTB-1703-01], the ADEME (French Environment and Energy Management Agency) [PROLIPHYT 1172C0053], the Région Franche-Comté [Environnement-Homme-Territoire 2014-069], the Pays de Montbéliard Agglomération [13/070-203-2015], and the French national program EC2CO-MicrobiEen FREIDI-Hg. A.D. received a PhD grant from the Région Franche-Comté.

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Durand, A., Maillard, F., Foulon, J. et al. Environmental Metabarcoding Reveals Contrasting Belowground and Aboveground Fungal Communities from Poplar at a Hg Phytomanagement Site. Microb Ecol 74, 795–809 (2017). https://doi.org/10.1007/s00248-017-0984-0

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