title: Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential.
abstract: Arbuscular mycorrhizal fungi (AMF) occur in the rhizosphere and in plant tissues as obligate symbionts, having key roles in plant evolution and nutrition. AMF possess endobacteria, and genome sequencing of the endobacterium Candidatus Glomeribacter gigasporarum revealed a reduced genome and a dependence on the fungal host. To understand the effect of bacteria on fungal fitness, we used next-generation sequencing to analyse the transcriptional profile of Gigaspora margarita in the presence and in the absence of its endobacterium. Genomic data on AMF are limited; therefore, we first generated a gene catalogue for G. margarita. Transcriptome analysis revealed that the endobacterium has a stronger effect on the pre-symbiotic phase of the fungus. Coupling transcriptomics with cell biology and physiological approaches, we demonstrate that the bacterium increases the fungal sporulation success, raises the fungal bioenergetic capacity, increasing ATP production, and eliciting mechanisms to detoxify reactive oxygen species. By using TAT peptide to translocate the bioluminescent calcium reporter aequorin, we demonstrated that the line with endobacteria had a lower basal intracellular calcium concentration than the cured line. Lastly, the bacteria seem to enhance the fungal responsiveness to strigolactones, the plant molecules that AMF perceive as branching factors. Although the endobacterium exacts a nutritional cost on the AMF, endobacterial symbiosis improves the fungal ecological fitness by priming mitochondrial metabolic pathways and giving the AMF more tools to face environmental stresses. Thus, we hypothesise that, as described for the human microbiota, endobacteria may increase AMF innate immunity.
authors.affiliation: Department of Life Science and Systems Biology, University of Torino, Torino, Italy.
authors.forename: Alessandra
authors.initials: A
authors.lastname: Salvioli
authors.affiliation: Institute for Sustainable Plant Protection (IPSP) - CNR, Torino, Italy.
authors.forename: Stefano
authors.identifier: http://orcid.org/0000-0002-2033-2286
authors.initials: S
authors.lastname: Ghignone
authors.affiliation: Department of Life Science and Systems Biology, University of Torino, Torino, Italy.
authors.forename: Mara
authors.identifier: http://orcid.org/0000-0001-7412-8750
authors.initials: M
authors.lastname: Novero
authors.affiliation: Department of Biology, University of Padova, Padova, Italy.
authors.forename: Lorella
authors.initials: L
authors.lastname: Navazio
authors.affiliation: Department of Life Science and Systems Biology, University of Torino, Torino, Italy.
authors.forename: Francesco
authors.initials: F
authors.lastname: Venice
authors.affiliation: Research Center for Genomics and Postgenomics, CRA-Fiorenzuola d'Arda, Italy.
authors.forename: Paolo
authors.initials: P
authors.lastname: Bagnaresi
authors.affiliation: Department of Life Science and Systems Biology, University of Torino, Torino, Italy.
authors.forename: Paola
authors.initials: P
authors.lastname: Bonfante
mesh_terms: D042521:Burkholderiaceae / Q000235:genetics / Q000502:physiology*; D004734:Energy Metabolism; D055137:Glomeromycota / Q000235:genetics / Q000502:physiology*; D053858:Metabolic Networks and Pathways; D038821:Mycorrhizae / Q000235:genetics / Q000502:physiology*; D013559:Symbiosis