title: Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria.
abstract: The recent accumulation of newly discovered fungal-bacterial mutualisms challenges the paradigm that fungi and bacteria are natural antagonists. To understand the mechanisms that govern the establishment and maintenance over evolutionary time of mutualisms between fungi and bacteria, we studied a symbiosis of the fungus Rhizopus microsporus (Mucoromycotina) and its Burkholderia endobacteria. We found that nonhost R. microsporus, as well as other mucoralean fungi, interact antagonistically with endobacteria derived from the host and are not invaded by them. Comparison of gene expression profiles of host and nonhost fungi during interaction with endobacteria revealed dramatic changes in expression of lipid metabolic genes in the host. Analysis of the host lipidome confirmed that symbiosis establishment was accompanied by specific changes in the fungal lipid profile. Diacylglycerol kinase (DGK) activity was important for these lipid metabolic changes, as its inhibition altered the fungal lipid profile and caused a shift in the host-bacterial interaction into an antagonism. We conclude that adjustments in host lipid metabolism during symbiosis establishment, mediated by DGKs, are required for the mutualistic outcome of the Rhizopus-Burkholderia symbiosis. In addition, the neutral and phospholipid profiles of R. microsporus provide important insights into lipid metabolism in an understudied group of oleaginous Mucoromycotina. Lastly, our study revealed that the DGKs involved in the symbiosis form a previously uncharacterized clade of DGK domain proteins.
authors.affiliation: Graduate Field of Microbiology, Cornell University, Ithaca, NY 14853.
authors.forename: Olga A
authors.initials: OA
authors.lastname: Lastovetsky
authors.affiliation: Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853.
authors.forename: Maria L
authors.initials: ML
authors.lastname: Gaspar
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598.
authors.forename: Stephen J
authors.initials: SJ
authors.lastname: Mondo
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598.
authors.forename: Kurt M
authors.initials: KM
authors.lastname: LaButti
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598.
authors.forename: Laura
authors.initials: L
authors.lastname: Sandor
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598.
authors.forename: Igor V
authors.initials: IV
authors.lastname: Grigoriev
authors.affiliation: Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853.
authors.forename: Susan A
authors.identifier: 0000-0002-2386-5184
authors.initials: SA
authors.lastname: Henry
authors.affiliation: School of Integrative Plant Science, Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, NY 14853 tep8@cornell.edu.
authors.forename: Teresa E
authors.initials: TE
authors.lastname: Pawlowska
mesh_terms: D005075:Biological Evolution; D019117:Burkholderia / Q000378:metabolism*; D019852:Diacylglycerol Kinase / Q000378:metabolism; D015966:Gene Expression Regulation, Fungal; D005819:Genetic Markers; D050356:Lipid Metabolism; D008055:Lipids / Q000737:chemistry; D020935:MAP Kinase Signaling System; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D012233:Rhizopus / Q000235:genetics*; D013559:Symbiosis; D015854:Up-Regulation
chemical_list: D005819:Genetic Markers; D008055:Lipids; D019852:Diacylglycerol Kinase
keywords: Mucoromycotina; Rhizopus–Burkholderia symbiosis; antagonism; mutualism evolution; oleaginous fungi