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Fungal and bacterial community responses to Suillus variegtus extraradical mycelia and soil profile in Scots pine microcosms

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Abstract

Aims

To investigate the importance of ectomycorrhizal (ECM) extraradical mycelia and soil substrate in shaping specific mycorrhizosphere microbial communities.

Methods

Suillus variagtus inoculated Scots pine seedlings were grown for approximately 5 months in soil microcosms using five soil layer treatments. Fungal and bacterial community composition near roots, in hyphal fronts and ‘bulk soil’ was studied using T-RFLP, cloning and sequencing. Plant chemistry at harvest and initial chemical properties for the soil layers were analysed.

Results

Both fungal and bacterial community compositions differed between different soil layers for S. variegatus inoculated seedlings. The mixed soil, corresponding to the interface between organic and mineral layers, supported the highest plant and fungal biomass and the most diverse fungal communities. Environmental variables explained ca. 50 % of the variation in data. In OE mixed layers the main driver shaping communities was plant chemistry, reflecting belowground C flow, and for O and E layers soil chemistry (nutrients and pH) was the main driver. Fungal communities included 56 identified taxa, and more taxa were found in soil associated with hyphal fronts compared to ‘bulk soil’ and roots. Bacterial communities changed over time and bacteria associated with hyphal fronts partly differentiated from other sampling sites.

Conclusion

The experimental microcosm setup allowed establishment of communities reflecting those naturally occurring at the field site. Given that belowground C flow is sufficient, extraradical mycelial expansion in the substrate has the potential to drive microbial community development.

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References

  • Agnelli A, Ascher J, Corti G, Ceccherini MT, Nannipieri P, Pietramellara G (2004) Distribution of microbial communities in a forest soil profile investigated by microbial biomass, soil respiration and DGGE of total and extracellular DNA. Soil Biol Biochem 36(5):859–868. doi:10.1016/j.soilbio.2004.02.004

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nuc Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389

    Article  CAS  Google Scholar 

  • Bahr A, Ellstrom M, Akselsson C, Ekblad A, Mikusinska A, Wallander H (2013) Growth of ectomycorrhizal fungal mycelium along a Norway spruce forest nitrogen deposition gradient and its effect on nitrogen leakage. Soil Biol Biochem 59:38–48. doi:10.1016/j.soilbio.2013.01.004

    Article  CAS  Google Scholar 

  • Bomberg M, Jurgens G, Saano A, Sen R, Timonen S (2003) Nested PCR detection of Archaea in defined compartments of pine mycorrhizaospheres developed in boreal forest humus microcosms. FEMS Microbiol Ecol 43:163–171

    Article  PubMed  CAS  Google Scholar 

  • Cairney JWG, Meharg AA (2002) Interactions between ectomycorrhizal fungi and soil saprotrophs: implications for decomposition of organic matter in soils and degradation of organic pollutants in the rhizosphere. Can J Bot Revue Canadienne De Botanique 80(8):803–809. doi:10.1139/b02-072

    Google Scholar 

  • Cebron A, Louvel B, Faure P, France-Lanord C, Chen Y, Murrell JC, Leyval C (2011) Root exudates modify bacterial diversity of phenanthrene degraders in PAH-polluted soil but not phenanthrene degradation rates. Environ Microbiol 13(3):722–736. doi:10.1111/j.1462-2920.2010.02376.x

    Article  PubMed  CAS  Google Scholar 

  • Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535. doi:10.1046/j.1469-8137.2002.00535.x

    Article  CAS  Google Scholar 

  • Duddridge JA (1986) The development and ultrastructure of ectomycorrhizas. III. Compatible and incompatible interactions between Suillus grevillei (Klotzsch) sing. and 11 species of ectomycorrhizal hosts in vitro in the absence of exogenous carbohydrate. New Phytol 103(3):457–465

    Article  CAS  Google Scholar 

  • Eilers KG, Debenport S, Anderson S, Fierer N (2012) Digging deeper to find unique microbial communities: The strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol Biochem 50:58–65. doi:10.1016/j.soilbio.2012.03.011

    Article  CAS  Google Scholar 

  • Ekblad A, Näsholm T (1996) Determination of chitin in fungi and mycorrhizal roots by an improved HPLC analysis of glucosamine. Plant Soil 178:29–35. doi:10.1007/bf00011160

    Article  CAS  Google Scholar 

  • Fitzjohn RG, Dickie IA (2007) TRAMPR: an R package for analysis and matching of terminal-restriction fragment length polymorphism (TRFLP) profiles. Mol Ecol Notes 7(4):583–587. doi:10.1111/j.1471-8286.2007.01744.x, Version 1.0-6

    Article  CAS  Google Scholar 

  • Fransson PMA, Johansson EM (2010) Elevated CO2 and nitrogen influence exudation of soluble organic compounds by ectomycorrhizal root systems. FEMS Microbiol Ecol 71(2):186–196. doi:10.1111/j.1574-6941.2009.00795.x

    Article  PubMed  CAS  Google Scholar 

  • Frey-Klett P, Chavatte M, Clausse ML, Courrier S, Le Roux C, Raaijmakers J, Martinotti MG, Pierrat JC, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165(1):317–328. doi:10.1111/j.1469-8137.2004.01212.x

    Article  PubMed  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. doi:10.1111/j.1365-294X.1993.tb00005.x

    Article  PubMed  CAS  Google Scholar 

  • Heinonsalo J, Sen R (2007) Scots pine ectomycorrhizal fungal inoculum potential and dynamics in podzol-specific humus, eluvial and illuvial horizons one and 4 years after forest clear-cut logging. Can J For Res 37:404–414. doi:10.1139/X06-212

    Article  CAS  Google Scholar 

  • Heinonsalo J, Hurme K-R, Sen R (2004) Recent 14C-labelled assimilate allocation to Scots pine seedling root and mycorrhizasphere compartments developed on reconstructed podzol humus, E- and B-horizons. Plant Soil 259:111–121. doi:10.1023/B:PLSO.0000020939.64205.c4

    Article  CAS  Google Scholar 

  • Heinonsalo J, Jørgensen KS, Sen R (2001) Microcosm-based analyses of Scots pine seedling growth, ectomycorrhizal fungal community structure and bacterial carbon utilization profiles in boreal forest humus and underlying illuvial minerla horizons. FEMS Micobial Ecol 36:73–84

    Article  CAS  Google Scholar 

  • Hobbie EA (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology 87(3):563–569

    Article  PubMed  Google Scholar 

  • Hynes HM, Germida JJ (2013) Impact of clear cutting on soil microbial communities and bioavailable nutrients in the LFH and Ae horizons of Boreal Plain forest soils. For Ecol Manag 306:88–95. doi:10.1016/j.foreco.2013.06.006

    Article  Google Scholar 

  • Ihrmark K, Bodeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandstrom-Durling M, Clemmensen KE, Lindahl BD (2012) New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. Fems Microbiol Ecol 82(3):666–677. doi:10.1111/j.1574-6941.2012.01437.x

    Article  PubMed  CAS  Google Scholar 

  • Izumi H, Elfstrand M, Fransson P (2013) Suillus mycelia under elevated atmospheric CO2 support increased bacterial communities and scarce nifH gene activity in contrast to Hebeloma mycelia. Mycorrhiza 23(2):155–165. doi:10.1007/s00572-012-0460-0

    Article  PubMed  CAS  Google Scholar 

  • Johansson EM, Fransson PMA, Finlay RD, van Hees PAW (2008) Quantitative analysis of root and ectomycorrhizal exudates as a response to Pb, Cd and As stress. Plant Soil 313(1–2):39–54. doi:10.1007/s11104-008-9678-1

    Article  CAS  Google Scholar 

  • Johansson EM, Fransson PMA, Finlay RD, van Hees PAW (2009) Quantitative analysis of soluble exudates produced by ectomycorrhizal roots as a response to ambient and elevated CO2. Soil Biol Biochem 41(6):1111–1116. doi:10.1016/j.soilbio.2009.02.016

    Article  CAS  Google Scholar 

  • Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166(2):247–257

    Article  CAS  Google Scholar 

  • Jumpponen A, Jones KL, Blair J (2010) Vertical distribution of fungal communities in tallgrass prairie soil. Mycologia 102(5):1027–1041. doi:10.3852/09-316

    Article  PubMed  Google Scholar 

  • Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E (2003) Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microbiol 69(1):327–333. doi:10.1128/aem.69.1.327-333.2003

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Hogberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173(3):611–620. doi:10.1111/j.1469-8137.2006.01936.x

    Article  PubMed  CAS  Google Scholar 

  • Lindahl BD, de Boer W, Finlay RD (2010) Disruption of root carbon transport into forest humus stimulates fungal opportunists at the expense of mycorrhizal fungi. ISME J 4:872–881

    Article  PubMed  Google Scholar 

  • Lundström US, van Breemen N, Bain D (2000) The podzolization process. A review. Geoderma 94(2–4):91–107. doi:10.1016/s0016-7061(99)00036-1

    Article  Google Scholar 

  • Marx DH (1969) Influence of ectotrophic mycorrhizal fungi on resistance of pine roots to pathogenic infections. I Antagonism of mycorrhizal fungi to root pathogenic fungi and soil bacteria. Phytopathol 59(2):153–163

    Google Scholar 

  • McCune B, Mefford MJ (2006) PC-ORD. Multivariate Analysis of Ecological Data. Version 5.33d, MjM Software Design, Gleneden Beach, Oregon, USA

  • McCune B, Grace JB (2002) Analysis of ecological communitites. MjM Software Design, Gleneden Beach, Oregon, USA. ISBN 0-9721290-0-6

    Google Scholar 

  • Osborne CA, Galic M, Sangwan P, Janssen PH (2005) PCR-generated artefact from 16S rRNA gene-specific primers. FEMS Microbiol Lett 248:183–187

    Article  PubMed  CAS  Google Scholar 

  • Pennanen T, Liski J, Baath E, Kitunen V, Uotila J, Westman CJ, Fritze H (1999) Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38(2):168–179

    Article  PubMed  Google Scholar 

  • Persson T (1980) Structure and function of northern coniferous forests – an ecosystem study. Ecol Bull 32. Stockholm, Sweden. ISSN: 0346–6868

  • Pickles BJ, Pither J (2013) Still scratching the surface: how much of the “black box” of soil ectomycorrhizal communities remains in the dark? New Phytol. doi:10.1111/nph.12616

    PubMed  Google Scholar 

  • Prescott CE, Greyston SJ (2013) Tree species influence on microbial communities in litter and soil: Current knowledge and research needs. For Ecol Man 309:19–27. doi:10.1016/j.foreco.2013.02.034

    Article  Google Scholar 

  • Rosling A, Landeweert R, Lindahl BD, Larsson KH, Kuyper TW, Taylor AFS, Finlay RD (2003) Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol 159(3):775–783. doi:10.1046/j.1469-8137.2003.00829.x

    Article  CAS  Google Scholar 

  • Rousk J, Bååth E (2007) Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique. Soil Biol Biochem 39(8):2173–2177. doi:10.1016/j.soilbio.2007.03.023

    Article  CAS  Google Scholar 

  • Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. Isme J 4(10):1340–1351. doi:10.1038/ismej.2010.58

    Article  PubMed  Google Scholar 

  • Rousk J, Brookes PC, Bååth E (2009) Contrasting Soil pH Effects on Fungal and Bacterial Growth Suggest Functional Redundancy in Carbon Mineralization. Appl Environ Microbiol 75(6):1589–1596. doi:10.1128/aem.02775-08

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Söderström B (2002) Challenges for mycorrhizal research into the new millennium. Plant Soil 244(1–2):1–7

    Article  Google Scholar 

  • Sun YP, Unestam T, Lucas SD, Johanson KJ, Kenne L, Finlay R (1999) Exudation-reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and soil microorganisms. Mycorrhiza 9(3):137–144

    Article  CAS  Google Scholar 

  • Timonen S, Jorgensen KS, Haahtela K, Sen R (1998) Bacterial community structure at defined locations of Pinus sylvestris Suillus bovinus and Pinus sylvestris Paxillus involutus mycorrhizospheres in dry pine forest humus and nursery peat. Can J Microbiol 44(6):499–513. doi:10.1139/cjm-44-6-499

    Article  CAS  Google Scholar 

  • Timonen S, Hurek T (2006) Characterization of culturable bacterial populations associating with Pinus sylvstris – Suillus bovinus mycorrhizospheres. Can J Microbiol 52:769–778. doi:10.1139/W06-016

    Article  PubMed  CAS  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(2):295–304. doi:10.1111/j.1574-6941.2007.00337.x

    Article  PubMed  CAS  Google Scholar 

  • Uroz S, Courty PE, Pierrat JC, Peter M, Buee M, Turpault MP, Garbaye J, Frey-Klett P (2013) Functional Profiling and Distribution of the Forest Soil Bacterial Communities Along the Soil Mycorrhizosphere Continuum. Microb Ecol 66(2):404–415. doi:10.1007/s00248-013-0199-y

    Article  PubMed  CAS  Google Scholar 

  • Uroz S, Turpault MP, Delaruelle C, Mareschal L, Pierrat JC, Frey-Klett P (2012) Minerals Affect the Specific Diversity of Forest Soil Bacterial Communities. Geomicrobiol J 29(1):88–98. doi:10.1080/01490451.2010.523764

    Article  CAS  Google Scholar 

  • Uroz S, Turpault MP, Van Scholl L, Palin B, Frey-Klett P (2011) Long term impact of mineral amendment on the distribution of the mineral weathering associated bacterial communities from the beech Scleroderma citrinum ectomycorrhizosphere. Soil Biol Biochem 43(11):2275–2282. doi:10.1016/j.soilbio.2011.07.010

    Article  CAS  Google Scholar 

  • van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundstomd US (2005) The carbon we do not see - the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37(1):1–13. doi:10.1016/j.soilbio.2004.06.010

    Article  CAS  Google Scholar 

  • Wallander H (1995) A new hypothesis top explain allocation of dry-matter between mycorrhizal fungi and pine-seedlings in relation to nutrient supply. Plant Soil 168:243–248. doi:10.1007/bf00029334

    Article  Google Scholar 

  • Wallander H, Nilsson LO, Hagerberg D, Baath E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151(3):753–760

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, (eds) PCR protocols: a guide to method and applications. Academic Press, San Diego, CA, USA, pp 315–322. ISBN: 0-12-372180-6\0-12-372181-4

  • Yao HY, Campbell CD, Chapman SJ, Freitag TE, Nicol GW, Singh BK (2013) Multi-factorial drivers of ammonia oxidizer communities: evidence from a national soil survey. Environ Microbiol 15(9):2545–2556. doi:10.1111/1462-2920.12141

    Article  PubMed  CAS  Google Scholar 

  • Zhu X, Cai J, Yang J, Su Q (2005) Determination of glucosamine in impure chitin samples by high-performance liquid chromatography. Carbohydr Res 340:1732–1738. doi:10.1016/j.carres.2005.01.045

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

We would like to thank the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) and The Royal Swedish Academy of Agriculture and Forestry (KSLA) for financial support. We thank Katarina Ihrmark for reading and commenting on the manuscript, and greatly appreciate the work done by the referees in providing feedback on the manuscript.

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Authors and Affiliations

  1. Uppsala BioCenter, Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden

    Petra Fransson

  2. Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden

    Anna Rosling

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  1. Petra Fransson
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  2. Anna Rosling
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Correspondence to Petra Fransson.

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Responsible Editor: Angela Hodge.

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Fransson, P., Rosling, A. Fungal and bacterial community responses to Suillus variegtus extraradical mycelia and soil profile in Scots pine microcosms. Plant Soil 385, 255–272 (2014). https://doi.org/10.1007/s11104-014-2231-5

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