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Front. Microbiol. | doi: 10.3389/fmicb.2019.00168

Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability

 Stefan Gorka1,  Marlies Dietrich1, Werner Mayerhofer1, Raphael Gabriel1, 2, Julia Wiesenbauer1, Victoria Martin1, Qing Zheng1, Bruna Imai1, Judith Prommer1,  Marieluise Weidinger1, Peter Schweiger1, Stephanie A. Eichorst1,  Michael Wagner1,  Andreas Richter1,  Arno Schintlmeister1,  Dagmar Woebken1* and  Christina Kaiser1*
  • 1Department of Microbiology and Ecosystem Science, University of Vienna, Austria
  • 2Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, United States Department of Energy (DOE), United States

Plant roots release recent photosynthates into the rhizosphere, accelerating decomposition of organic matter by saprotrophic soil microbes (’rhizosphere priming effect’) which consequently increases nutrient availability for plants. However, about 90% of all higher plant species are mycorrhizal, transferring a significant fraction of their photosynthates directly to their fungal partners. Whether mycorrhizal fungi pass on plant-derived carbon (C) to bacteria in root-distant soil areas, i.e. incite a ‘hyphosphere priming effect’, is not known. Experimental evidence for C transfer from mycorrhizal hyphae to soil bacteria is limited, especially for ectomycorrhizal systems. As ectomycorrhizal fungi possess enzymatic capabilities to degrade organic matter themselves, it remains unclear whether they cooperate with soil bacteria by providing photosynthates, or compete for available nutrients.

To investigate a possible C transfer from ectomycorrhizal hyphae to soil bacteria, and its response to changing nutrient availability, we planted young beech trees (Fagus sylvatica) into ‘split-root’ boxes, dividing their root systems into two disconnected soil compartments. Each of these compartments was separated from a litter compartment by a mesh penetrable for fungal hyphae, but not for roots. Plants were exposed to a 13C-CO2–labeled atmosphere, while 15N-labeled ammonium and amino acids were added to one side of the split-root system.

We found a rapid transfer of recent photosynthates via ectomycorrhizal hyphae to bacteria in root-distant soil areas. Fungal and bacterial phospholipid fatty acid (PLFA) biomarkers were significantly enriched in hyphae-exclusive compartments 24 h after 13C-CO2–labeling. Isotope imaging with nanometer-scale secondary ion mass spectrometry (NanoSIMS) allowed for the first time in situ visualization of plant-derived C and N taken up by extraradical fungal hyphae, and in microbial cells thriving on hyphal surfaces. When N was added to the litter compartments, bacterial biomass and the amount of incorporated 13C strongly declined. Interestingly, this effect was also observed in adjacent soil compartments where added N was only available for bacteria through hyphal transport, indicating that ectomycorrhizal fungi were acting on soil bacteria. Together, our results demonstrate that (i) ectomycorrhizal hyphae rapidly transfer plant-derived C to bacterial communities in root-distant areas, and (ii) this transfer promptly responds to changing soil nutrient conditions.

Keywords: hyphal C transfer, hyphosphere bacteria, Mycorrhizosphere, hyphosphere priming, NanoSIMS, Tripartite symbiosis, Fungal-bacterial interactions, Ectomycorrhiza (EcM)

Received: 10 Aug 2018; Accepted: 22 Jan 2019.

Edited by:

Tim Daniell, James Hutton Institute, United Kingdom

Reviewed by:

Rodica Pena, University of Göttingen, Germany
Gary D. Bending, University of Warwick, United Kingdom
Katie Field, University of Leeds, United Kingdom  

Copyright: © 2019 Gorka, Dietrich, Mayerhofer, Gabriel, Wiesenbauer, Martin, Zheng, Imai, Prommer, Weidinger, Schweiger, Eichorst, Wagner, Richter, Schintlmeister, Woebken and Kaiser. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Dagmar Woebken, University of Vienna, Department of Microbiology and Ecosystem Science, Vienna, Austria, woebken@microbial-ecology.net
Dr. Christina Kaiser, University of Vienna, Department of Microbiology and Ecosystem Science, Vienna, Austria, christina.kaiser@univie.ac.at