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Journal Articles Current Biology - CB Year : 2021

Symbiotic nitrogen fixation in the reproductive structures of a basidiomycete fungus

Rachel Koch
  • Function : Author
Gyeong Mee Yoon
  • Function : Author
Uma Aryal
  • Function : Author
Kathleen Lail
  • Function : Author
Mojgan Amirebrahimi
  • Function : Author
Kurt Labutti
Anna Lipzen
Robert Riley
  • Function : Author
Kerrie Barry
Igor Grigoriev
Joshua Herr
  • Function : Author
M Catherine Aime
  • Function : Author
M. Catherine Aime
  • Function : Author


Nitrogen (N) fixation is a driving force for the formation of symbiotic associations between N2-fixing bacteria and eukaryotes.1 Limited examples of these associations are known in fungi, and none with sexual structures of non-lichenized species.2-6 The basidiomycete Guyanagaster necrorhizus is a sequestrate fungus endemic to the Guiana Shield.7 Like the root rot-causing species in its sister genera Armillaria and Desarmillaria, G. necrorhizus sporocarps fruit from roots of decaying trees (Figures 1A-1C),8 and genome sequencing is consistent with observations that G. necrorhizus is a white-rotting decomposer. This species also represents the first documentation of an arthropod-dispersed sequestrate fungus. Numerous species of distantly related wood-feeding termites, which scavenge for N-rich food, feed on the mature spore-bearing tissue, or gleba, of G. necrorhizus. During feeding, mature spores adhere to termites for subsequent dispersal.9 Using chemical assays, isotope analysis, and high-throughput sequencing, we show that the sporocarps harbor actively N2-fixing Enterobacteriaceae species and that the N content within fungal tissue increases with maturation. Untargeted proteomic profiling suggests that ATP generation in the gleba is accomplished via fermentation. The use of fermentation-an anaerobic process-indicates that the sporocarp environment is anoxic, likely an adaptation to protect the oxygen-sensitive nitrogenase enzyme. Sporocarps also have a thick outer covering, possibly to limit oxygen diffusion. The enriched N content within mature sporocarps may offer a dietary inducement for termites in exchange for spore dispersal. These results show that the flexible metabolic capacity of fungi may facilitate N2-fixing associations, as well as higher-level organismal associations.

Dates and versions

hal-03353944 , version 1 (24-09-2021)



Rachel Koch, Gyeong Mee Yoon, Uma Aryal, Kathleen Lail, Mojgan Amirebrahimi, et al.. Symbiotic nitrogen fixation in the reproductive structures of a basidiomycete fungus. Current Biology - CB, 2021, 31 (17), pp.3905-3914.e6. ⟨10.1016/j.cub.2021.06.033⟩. ⟨hal-03353944⟩
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