Symbiotic nitrogen fixation in the reproductive structures of a basidiomycete fungus

Rachel A Koch; Gyeong Mee Yoon; Uma K Aryal; Kathleen Lail; Mojgan Amirebrahimi; Kurt LaButti; Anna Lipzen; Robert Riley; Kerrie Barry; Bernard Henrissat; Igor V Grigoriev; Joshua R Herr; M Catherine Aime

doi:10.1016/j.cub.2021.06.033

Symbiotic nitrogen fixation in the reproductive structures of a basidiomycete fungus

Curr Biol. 2021 Sep 13;31(17):3905-3914.e6. doi: 10.1016/j.cub.2021.06.033. Epub 2021 Jul 9.

Authors

Affiliations

¹ Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA; Department of Plant Pathology, University of Nebraska, Lincoln, NE 68520, USA. Electronic address: rachelannekoch@gmail.com.
² Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA.
³ Purdue Proteomics Facility, Bindley Bioscience Center, Purdue University, West Lafayette, IN 47907, USA; Department of Comparative Pathobiology, Purdue University, West Lafayette, IN 47907, USA.
⁴ US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
⁵ Architecture et Fonction des Macromolécules Biologiques, CNRS, Aix-Marseille Université, Marseille 13288, France; Institut National de la Recherche Agronomique, USC1408 Architecture et Fonction des Macromolécules Biologiques, Marseille 13288, France; Department of Biological Sciences, King Abdulaziz University, Jeddah 21589, Saudi Arabia.
⁶ US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA; Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA 94720, USA.
⁷ Department of Plant Pathology, University of Nebraska, Lincoln, NE 68520, USA; Center for Plant Science Innovation, University of Nebraska, Lincoln, NE 68520, USA.
⁸ Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA. Electronic address: maime@purdue.edu.

PMID: 34245690
DOI: 10.1016/j.cub.2021.06.033

Abstract

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.

Keywords: Basidiomycota; Enterobacteriaceae; Guiana Shield; Physalacriaceae; genome sequencing; insect fungiculture; mutualism; trophic interactions; tropical ecology; white rot.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Basidiomycota* / genetics
Isoptera* / microbiology
Nitrogen
Nitrogen Fixation
Proteomics
Symbiosis

Substances

Nitrogen