Exo‐ and endophytic fungi enable rapid transfer of nutrients from ant waste to orchid tissue

Author:

Gegenbauer Christian12ORCID,Bellaire Anke1,Schintlmeister Arno3ORCID,Schmid Markus C.3,Kubicek Markus4ORCID,Voglmayr Hermann56ORCID,Zotz Gerhard78ORCID,Richter Andreas2ORCID,Mayer Veronika E.1ORCID

Affiliation:

1. Division of Structural and Functional Botany, Department of Botany and Biodiversity Research University of Vienna Rennweg 14 1030 Wien Austria

2. Division of Terrestrial Ecosystem Research, Centre for Microbiology and Ecosystem Science University of Vienna Djerassiplatz 1 1030 Wien Austria

3. Division of Microbial Ecology and Large‐Instrument Facility of Environmental and Isotope Mass Spectrometry, Centre for Microbiology and Environmental Systems Science University of Vienna Djerassiplatz 1 1030 Vienna Austria

4. Institute of Chemical Technologies and Analytics, TU Wien Getreidemarkt 9/164 1060 Vienna Austria

5. Mycology Research Group, Department of Botany and Biodiversity Research University of Vienna Rennweg 14 1030 Wien Austria

6. Institute of Forest Entomology, Forest Pathology and Forest Protection University of Natural Resources and Life Sciences, Vienna (BOKU) Peter‐Jordan‐Strasse 82 1190 Wien Austria

7. Institute for Biology and Environmental Sciences Carl von Ossietzky University Oldenburg Oldenburg Germany

8. Smithsonian Tropical Research Institute Apdo 2072 Balboa Panama

Abstract

Summary The epiphytic orchid Caularthron bilamellatum sacrifices its water storage tissue for nutrients from the waste of ants lodging inside its hollow pseudobulb. Here, we investigate whether fungi are involved in the rapid translocation of nutrients. Uptake was analysed with a 15N labelling experiment, subsequent isotope ratio mass spectrometry (IRMS) and secondary ion mass spectrometry (ToF‐SIMS and NanoSIMS). We encountered two hyphae types: a thick melanized type assigned to ‘black fungi’ (Chaetothyriales, Cladosporiales, and Mycosphaerellales) in ant waste, and a thin endophytic type belonging to Hypocreales. In few cell layers, both hyphae types co‐occurred. 15N accumulation in both hyphae types was conspicuous, while for translocation to the vessels only Hypocreales were involved. There is evidence that the occurrence of the two hyphae types results in a synergism in terms of nutrient uptake. Our study provides the first evidence that a pseudobulb (=stem)‐born endophytic network of Hypocreales is involved in the rapid translocation of nitrogen from insect‐derived waste to the vegetative and reproductive tissue of the host orchid. For C. bilamellatum that has no contact with the soil, ant waste in the hollow pseudobulbs serves as equivalent to soil in terms of nutrient sources.

Funder

Austrian Science Fund

Universität Wien

Publisher

Wiley

Subject

Plant Science,Physiology

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