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Emilia  Hannula's picture

Dr. Emilia Hannula

Researcher

Terrestrial Ecology


Research themes
  • Microbiomes
  • Restoration ecology

  • Research expertise
  • Belowground interactions
  • Molecular techniques and bioinformatic analyis (NGS)
  • Soil fungal communities
  • Stable isotope probing

  • Page last updated: 12-01-2021

    I love soil fungi! And am lucky enough to be able to work with these creatures and explain the world how important fungi are for functioning of ecosystems. My main focus is on how soil fungal communities regulate plant communities and interact with so many other organisms indirectly or directly,

    • CV
    • Key publications
    • Peer-reviewed publications
    • Popular-scientific publications
    • Ancillary positions

    Education

    1.6. 2007, Master of Science degree in Ecology and Environmental Sciences, University of Helsinki, Finland
    Master thesis subject: The effect of diesel and its removal on the population dynamics of bacteria in the Baltic Sea. 
     
    17.10.2012, PhD degree in Microbial Ecology from University of Leiden, The Netherlands 
    Thesis subject: Assessment of the effects of genetically-modified potatoes on the structure and functioning of soil fungal communities.
     
    Research
     
    2012-2015, Post-doc, NIOO-KNAW, Department of Microbial Ecology,  Wageningen, The Netherlands
    Project: Fungal diversity and functioning in European soils in EcoFINDERS
     
    2016-2017, Researcher at Soil Cares Research, Wageningen, The Netherlands
     
    2017-2019, Post-doc at NIOO-KNAW, Department of Terrestrial Ecology
    Projects:
    Linking aboveground-belowground interactions and plant-soil-feedback to improve pest control and sustainability in greenhouse cut-flowers (see blog post about this project)
    Living legacies: Influence of plant-mediated changes in soil communities on aboveground plant-insect interactions

    Currently

    2019- Researcher at NIOO-KNAW, Department of Terrestrial Ecology
    Project:
    Learning from nature- towards sustainable crop production using soil fungi

     

    Blog posts related to current project

    Here we go!
    Searching for best soil in the Netherlands
    Life as an academic researcher
    Potatoes are ready!
     
    And some thoughts during lockdown: here

     

    And always: looking for students!

     

    Heinen, R.*, Hannula, S.E.*, De Long, J.R.*, Huberty, M., Jongen, R., Kielak, A., Steinauer, K., Zhu, F. and Bezemer, T.M. (2020), Plant community composition steers grassland vegetation via soil legacy effects. Ecology Letters 23: 973-982. doi:10.1111/ele.13497
    Here we show in a field-based manipulation that conditioning plant community – via effects on soil fungi – steer the composition of responding plant community. We show that the effects of observed are potentially driven by grass-specific plant pathogenic fungi.

    Hannula, S.E., Ma, H.K., Pérez-Jaramillo J.E., Pineda, A & Bezemer, T.M.: (2020) Structure and ecological function of the soil microbiome affecting plant-soil feedbacks in the presence of a soil-borne pathogen.  Environmental microbiology 22: 660-676. doi:10.1111/1462-2920.14882
    Here we conditioned soils with 37 plant species and relate it to performance of the following plant in absence and presence of pathogen. We show that microbiomes predict largely the performance of the following plant but that the composition of the micorbiome cannot be predicted by the functional group of the plant in conditioning phase. 

    Hannula, S.E., Kielak, A.M., Steinauer, K., Huberty, M., Jongen, R., De Long, J.R., Heinen, R., Bezemer, T.M. (2019) Time after time: temporal variation in the effects of plant species and plant functional groups on soil bacterial and fungal communities. mBio 10 (6): e02635-19
    In this article we show that bacterial communities change largely over time while fungal communities are more stable and affected more by the plants (and their functional groups) growing in the soils. 

    Hannula, S.E., Zhu, F., Heinen, R., Bezemer, T.M. (2019): Foliar-feeding insects acquire microbiomes from the soil rather than the host plant. Nature communications 10 (1), 1254
    In this article we identified microbiomes in the soils, inside plant roots and leaves and inside plant feeding caterpillars kept on both intact leaves and whole plants. We show that the legacy of past plant communities can be detected in the caterpillars kept on whole plants and that they share large part of their microbiome with soil indicating that they pick up their microbiome from the soil (rather than food sources). This opens a whole new research area and it will be interesting to study how food and environment affect development and performance of other insects. Furthermore, it will be interesting to study the transfer of microbiomes between trophic levels. 

    Hannula, S.E., Morriën, E., de Hollander, M., van der Putten, W.H., van Veen, J.A., de Boer, W. (2017): Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture. ISMEJ 11: 2294–2304
    In this article we show using stable isotopes combined with high-throughput sequencing (DNA-SIP) that rhizosphere fungal community function changes during secondary succession in grasslands taken out from agricultural production. We show a shift from yeast and pathogen rich community in early successional stages towards a mutualist rich communities in later successional stages and relate this to the fungal feeding organisms. 

    Hannula, S.E.*, Morriën, E.*, Snoek, L.B.,  Helmsing, N.R.,  Zweers, H.,  de Hollander, M.,  Luján Soto, R., Bouffaud, M.-L.,  Buée, M., Dimmers, W.,  Duyts, H.,  Geisen, S.,  Girlanda, M.,  Griffiths, R.I.,  Jørgensen, H.-B.,  Jensen, J.,  Plassart, P.,  Redecker, D.,  Schmelz, R.M.,  Schmidt, O.,  Thomson, B.C, Tisserant, E.,  Uroz, S.,  Winding, A.,  Bailey, M.J.,  Bonkowski, M.,  Faber, J.H.,  Martin, F.,  Lemanceau, P., de Boer, W.,  van Veen, J.A.,  van der Putten, W.H. (2017): Soil networks become more connected and take up more carbon as nature restoration progresses. Nature communications 8: 14349
    Using 13C labeling of intact soil cores and resolving the whole soil foodweb, we show that secondary succession of ex-arable fields leads to more connected soil communities that can store the carbon more efficiently. We also highlight that relative importance of fungi becomes bigger when longer time is past since agriculture and show that this leads to increased retention of carbon in the system. 

    Creamer, R.E., Hannula, S.E., van Leeuwen, J.P., Stone, D., Rutgers, M., Schmelz, R.M., de Ruiter, P.C., Bohse Hendriksen, N., Bolger, T., Bouffaud, M.-L., Buee, M., Carvalho, F., Costa, D., Dirilgen, T., Francisco, R., Griffiths, B.S., Martin, F., Martins da Silva, P., Mendes, S., Morais, P.V., Pereira , C., Philippot, L., Plassart, P., Redecker, D., Römbke, J., Sousa, J.P., Wouterse, M., Lemanceau, P., 2016. Ecological network analysis reveals the inter-connection between soil biodiversity and ecosystem function as affected by land use across Europe. (2015) Applied Soil Ecology 97 (112-124).
    This article is a result of large transect collected across Europe. Here we explore by using for example network analysis  the relationships between groups of soil biota change depending on land-use type and for example soil pH and that this could be related to ecosystem functions.

    Hannula S.E., Boschker HTS, de Boer W, van Veen JA. (2012). 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. New Phytologist 194(3): 784-799.  
    In this article we showed using 13C labeling of whole plants combined with PLFA-SIP and RNA-SIP that fungi are important component of soil microbiome in agricultural soils in terms of amount of carbon they receive from the plant especially at older stages of growth of the plant. This research sparked the idea to look into the role of fungi in agricultural systems in more detail. 
     

     

      2021

    • De Long, J., Heinen, R., Jongen, R., Hannula, E., Huberty, M. D., Kielak, A. M., Steinauer, K., & Bezemer, T. M. (2021). How plant-soil feedbacks influence the next generation of plants. Ecological Research, 36(1), 32-44. https://doi.org/10.1111/1440-1703.12165
    • Hannula, E., Di Lonardo, P., Christensen, B. T., Crotty, F. V., Elsen, A., Erp, P. J. V., Hansen, E. M., Rubæk, G. H., Tits, M., Tóth, Z., & Termorshuizen, A. J. (2021). Inconsistent effects of agricultural practices on soil fungal communities across twelve European long-term experiments. European Journal of Soil Science, in press. https://doi.org/10.1111/ejss.13090
    • 2020

    • Steinauer, K., Heinen, R., Hannula, E., De Long, J., Huberty, M. D., Jongen, R., Wang, M., & Bezemer, T. M. (2020). Above-belowground linkages of functionally dissimilar plant communities and soil properties in a grassland experiment. Ecosphere, 11(2020), [e03246]. https://doi.org/10.1002/ecs2.3246
    • Pineda, A. M., Kaplan, I., Hannula, E., Ghanem, W., & Bezemer, T. M. (2020). Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest. New Phytologist, 226(2), 595-608. https://doi.org/10.1111/nph.16385
    • Li, Y., Veen, G. F. C., Hol, W. H. G., Vandenbrande, S., Hannula, S. E., ten Hooven, F. C., Li, Q., Liang, W., & Bezemer, T. M. (2020). ‘Home’ and ‘away’ litter decomposition depends on the size fractions of the soil biotic community. Soil Biology & Biochemistry, 144, [107783]. https://doi.org/10.1016/j.soilbio.2020.107783
    • Fernandes Gomes, S. I., Kielak, A. M., Hannula, E., Heinen, R., Jongen, R., Keesmaat, I., De Long, J., & Bezemer, T. M. (2020). Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities. Animal Microbiome, 2, [37]. https://doi.org/10.1186/s42523-020-00055-3
    • Heinen, R., Hannula, E., De Long, J., Huberty, M. D., Jongen, R., Kielak, A. M., Steinauer, K., Zhu, F., & Bezemer, T. M. (2020). Plant community composition steers grassland vegetation via soil legacy effects. Ecology Letters, 23(6), 973-982. https://doi.org/10.1111/ele.13497
    • Hannula, E., Morrien, E., van der Putten, W. H., & de Boer, W. (2020). Rhizosphere fungi actively assimilating plant-derived carbon in a grassland soil. Fungal Ecology, 48, [100988]. https://doi.org/10.1016/j.funeco.2020.100988
    • Hannula, E., & Träger, S. (2020). Soil fungal guilds as important drivers of the plant richness–productivity relationship: (Invited) commentary. New Phytologist, 226(4), [947-949]. https://doi.org/10.1111/nph.16523
    • Pangesti, N., Pineda, A. M., Hannula, E., & Bezemer, T. M. (2020). Soil inoculation alters the endosphere microbiome of chrysanthemum roots and leaves. Plant and Soil, 455, 107-119. https://doi.org/10.1007/s11104-020-04655-5
    • Ma, H., Pineda, A. M., Hannula, E., Kielak, A. M., Setyarini, S. N., & Bezemer, T. M. (2020). Steering root microbiomes of a commercial horticultural crop with plant-soil feedbacks. Applied Soil Ecology, 150, [103468]. https://doi.org/10.1016/j.apsoil.2019.103468
    • Hannula, E., Ma, H., Perez Jaramillo, J. E., Pineda, A. M., & Bezemer, T. M. (2020). Structure and ecological function of the soil microbiome affecting plant-soil feedbacks in the presence of a soil-borne pathogen. Environmental Microbiology, 22(2), 660-676. https://doi.org/10.1111/1462-2920.14882
    • Clocchiatti, A., Hannula, E., Van den Berg, M., Korthals, G., & De Boer, W. (2020). The hidden potential of saprotrophic fungi in arable soil: patterns of short-term stimulation by organic amendments. Applied Soil Ecology, 147, [103434]. https://doi.org/10.1016/j.apsoil.2019.103434
    • 2019

    • Geisen, S., Briones, M. J. I., Gan, H., Behan-Pelletier, V. M., Friman, V-P., de Groot, G. A., Hannula, S. E., Lindo, Z., Philippot, L., Tiunov, A. V., & Wall, D. H. (2019). A methodological framework to embrace soil biodiversity. Soil Biology & Biochemistry, 136, [107536]. https://doi.org/10.1016/j.soilbio.2019.107536
    • Hannula, S. E., Zhu, F., Heinen, R., & Bezemer, T. M. (2019). Foliar-feeding insects acquire microbiomes from the soil rather than the host plant. Nature Communications, 10, [1254(2019)]. https://doi.org/10.1038/s41467-019-09284-w
    • Wang, M., Ruan, W., Kostenko, O., Carvalho, S., Hannula, S. E., Mulder, P. P. J., Bu, F., van der Putten, W. H., & Bezemer, T. M. (2019). Removal of soil biota alters soil feedback effects on plant growth and defense chemistry. New Phytologist, 221(3), 1478-1491. https://doi.org/10.1111/nph.15485
    • De Long, J. R., Heinen, R., Steinauer, K., Hannula, S. E., Huberty, M., Jongen, R., Vandenbrande, S., Wang, M., Zhu, F., & Bezemer, T. M. (2019). Taking plant-soil feedbacks to the field in a temperate grassland. Basic and Applied Ecology, in press, 30-42. https://doi.org/10.1016/j.baae.2019.08.001
    • Hannula, E., Kielak, A. M., Steinauer, K., Huberty, M. D., Jongen, R., De Long, J., Heinen, R., & Bezemer, T. M. (2019). Time after time: Temporal variation in the effects of grass and forb species on soil bacterial and fungal communities. mBio, 10, [02635-19]. https://doi.org/10.1128/mBio.02635-19
    • 2018

    • Frąc, M., Hannula, S. E., Bełka, M., & Jędryczka, M. (2018). Fungal Biodiversity and Their Role in Soil Health. Frontiers in Microbiology, 9, 707. [707]. https://doi.org/10.3389/fmicb.2018.00707
    • 2017

    • Di Lonardo, P., De Boer, W., Klein Gunnewiek, P. J. A., Hannula, S. E., & Van der Wal, A. (2017). Priming of soil organic matter: Chemical structure of added compounds is more important than the energy content. Soil Biology & Biochemistry, 108, 41-54. https://doi.org/10.1016/j.soilbio.2017.01.017
    • Hannula, S. E., Morriën, E., De Hollander, M., van der Putten, W. H., van Veen, J. A., & De Boer, W. (2017). Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture. ISME Journal, 11, 2294-2304. https://doi.org/10.1038/ismej.2017.90
    • Morriën, E., Hannula, S. E., Snoek, B., Helmsing, N. R., Zweers, H., De Hollander, M., Lujan Soto, R., Bouffaud, M. L., Buée, M., Dimmers, W., Duyts, H., Geisen, S., Girlanda, M., Griffiths, R. I., Jørgensen, H-B., Jensen, J., Plassart, P., Redecker, D., Schmelz, R. M.,... van der Putten, W. H. (2017). Soil networks become more connected and take up more carbon as nature restoration progresses. Nature Communications, 8, [14349]. https://doi.org/10.1038/ncomms14349
    • 2016

    • Creamer, R. E., Hannula, S. E., Leeuwen, J. P. V., Stone, D., Rutgers, M., Schmelz, R. M., Ruiter, P. C. D., Hendriksen, N. B., Bolger, T., Bouffaud, M. L., Buee, M., Carvalho, F., Costa, D., Dirilgen, T., Francisco, R., Griffiths, B. S., Griffiths, R., Martin, F., Silva, P. M. D.,... Lemanceau, P. (2016). Ecological network analysis reveals the inter-connection between soil biodiversity and ecosystem function as affected by land use across Europe. Applied Soil Ecology, 97, 112-124. https://doi.org/10.1016/j.apsoil.2015.08.006
    • Hannula, S. E., & van Veen, J. A. (2016). Primer Sets Developed for Functional Genes Reveal Shifts in Functionality of Fungal Community in Soils. Frontiers in Microbiology, 7, [fmicb.2016.01897]. https://doi.org/10.3389/fmicb.2016.01897
    • Griffiths, B. S., Römbke, J., Schmelz, R. M., Scheffczyk, A., Faber, J. H., Bloem, J., Pérès, G., Cluzeau, D., Chabbi, A., Suhadolc, M., Sousa, J. P., Martins Da Silva, P., Carvalho, F., Mendes, S., Morais, P., Francisco, R., Pereira, C., Bonkowski, M., Geisen, S.,... Stone, D. (2016). Selecting cost effective and policy-relevant biological indicators for European monitoring of soil biodiversity and ecosystem function. Ecological Indicators, 69, 213-223. https://doi.org/10.1016/j.ecolind.2016.04.023
    • 2015

    • Thomson, B. C., Tisserant, E., Plassart, P., Uroz, S., Griffiths, R. I., Hannula, S. E., Buée, M., Mougel, C., Ranjard, L., Van Veen, J. A., Martin, F., Bailey, M. J., & Lemanceau, P. (2015). Soil conditions and land use intensification effects on soil microbial communities across a range of European field sites. Soil Biology & Biochemistry, 88(September). https://doi.org/10.1016/j.soilbio.2015.06.012
    • 2014

    • Hannula, S. E., De Boer, W., & Van Veen, J. A. (2014). Do genetic modifications in crops affect soil fungi? a review. Biology and Fertility of Soils, 50(3), 433-446. https://doi.org/10.1007/s00374-014-0895-x
    • 2013

    • Franco Dias, A. C., Dini-Andreote, F., Hannula, S. E., de Cassia Pereira e Silva, M., Salles, J., De Boer, W., Van Veen, J. A., & Van Elsas, J. D. (2013). Different Selective Effects on Rhizosphere Bacteria Exerted by Genetically Modified versus Conventional Potato Lines. PLoS One, 8(7), [e67948]. https://doi.org/10.1371/journal.pone.0067948
    • Hannula, S. E., De Boer, W., Baldrian, P., & Van Veen, J. A. (2013). Effect of genetic modification of potato starch on decomposition of leaves and tubers and on fungal decomposer communities. Soil Biology & Biochemistry, 58, 88-98. https://doi.org/10.1016/j.soilbio.2012.11.008
    • 2012

    • Hannula, S. E., Boschker, H. T. S., De Boer, W., & Van Veen, J. A. (2012). 13C pulse-labeling assessment of the community structure of active fungi in the rhizosphere of a genetically starch-modified potato (Solanum tuberosum) cultivar and its parental isoline. New Phytologist, 194(3), 784-799. https://doi.org/10.1111/j.1469-8137.2012.04089.x
    • Hannula, S. E., De Boer, W., & Van Veen, J. A. (2012). A 3-year study reveals that plant growth stage, season and field site affect soil fungal communities while cultivar and GM-trait have minor effects. PLoS One, 7(4), [e33819]. https://doi.org/10.1371/journal.pone.0033819
    • Hannula, S. E. (2012). Assessment of the effects of genetically modified potatoes on structure and functioning of soil fungal communities (PhD Thesis). Leiden University Press. https://openaccess.leidenuniv.nl/handle/1887/19969
    • Brinkman, E. P., Raaijmakers, C. E., Bakx-Schotman, J. M. T., Hannula, S. E., Kemmers, R. H., De Boer, W., & Van der Putten, W. H. (2012). Matgrass sward plant species benefit from soil organisms. Applied Soil Ecology, 62, 61-70. https://doi.org/10.1016/j.apsoil.2012.07.012
    • 2010

    • Hannula, S. E., De Boer, W., & Van Veen, J. A. (2010). In situ dynamics of soil fungal communities under different genotypes of potato, including a genetically modified cultivar. Soil Biology & Biochemistry, 42(12), 2211-2223. https://doi.org/10.1016/j.soilbio.2010.08.020

      2018

    • Hannula, S. E., Ma, H., Pineda, A. M., & Bezemer, T. M. (2018). Sturen van bodemmicrobiomen voor plantgezondheid in de tuinbouw. Gewasbescherming, 66.
    • 2012

    • Hannula, S. E. (2012). The importance of fungi in the potato rhizosphere. Gewasbescherming, 43(4), 127-128. http://www.knpv.org/db/upload/documents/Gewasbescherming/2012gb43nr4.pdf
      Associate editor European Journal of Soil Science (2019 - current)

      Associate editor Journal of Applied Ecology (2020 - current)

    Contact

    +31 (0)317 473 580

    Droevendaalsesteeg 10
    6708 PB Wageningen 
    +31 (0)317 47 34 00

    Postbus 50 
    6700 AB Wageningen

    E.Hannula@nioo.knaw.nl

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