title: Horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal Amanita.
abstract: The genus Amanita encompasses both symbiotic, ectomycorrhizal fungi and asymbiotic litter decomposers; all species are derived from asymbiotic ancestors. Symbiotic species are no longer able to degrade plant cell walls. The carbohydrate esterases family 1 (CE1s) is a diverse group of enzymes involved in carbon metabolism, including decomposition and carbon storage. CE1 genes of the ectomycorrhizal A. muscaria appear diverged from all other fungal homologues, and more similar to CE1s of bacteria, suggesting a horizontal gene transfer (HGT) event. In order to test whether AmanitaCE1s were acquired horizontally, we built a phylogeny of CE1s collected from across the tree of life, and describe the evolution of CE1 genes among Amanita and relevant lineages of bacteria. CE1s of symbiotic Amanita were very different from CE1s of asymbiotic Amanita, and are more similar to bacterial CE1s. The protein structure of one CE1 gene of A. muscaria matched a depolymerase that degrades the carbon storage molecule poly((R)-3-hydroxybutyrate) (PHB). Asymbiotic Amanita do not carry sequence or structural homologues of these genes. The CE1s acquired through HGT may enable novel metabolisms, or play roles in signaling or defense. This is the first evidence for the horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal fungi.
authors.affiliation: Department of Microbial Ecology, University of Groningen, 9747 AG, Groningen, the Netherlands.|Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA.
authors.forename: Maryam
authors.identifier: http://orcid.org/0000-0002-3359-3258
authors.initials: M
authors.lastname: Chaib De Mares
authors.affiliation: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA.|Department of Biosciences, University of Oslo, 0371, Oslo, Norway.
authors.forename: Jaqueline
authors.initials: J
authors.lastname: Hess
authors.affiliation: Department of Biology, Clark University, Worcester, MA, 01610, USA.
authors.forename: Dimitrios
authors.initials: D
authors.lastname: Floudas
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA, 94598, USA.
authors.forename: Anna
authors.initials: A
authors.lastname: Lipzen
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA, 94598, USA.
authors.forename: Cindy
authors.initials: C
authors.lastname: Choi
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA, 94598, USA.
authors.forename: Megan
authors.initials: M
authors.lastname: Kennedy
authors.affiliation: US Department of Energy Joint Genome Institute, Walnut Creek, CA, 94598, USA.
authors.forename: Igor V
authors.initials: IV
authors.lastname: Grigoriev
authors.affiliation: Harvard Forest, 324 North Main Street, Petersham, MA, 01366, USA.
authors.forename: Anne
authors.initials: A
authors.lastname: Pringle
mesh_terms: D000545:Amanita / Q000201:enzymology / Q000235:genetics*; D050260:Carbohydrate Metabolism / Q000235:genetics*; D005656:Fungal Proteins / Q000737:chemistry / Q000235:genetics; D022761:Gene Transfer, Horizontal; D005800:Genes, Fungal; D008958:Models, Molecular; D038821:Mycorrhizae / Q000235:genetics*; D010802:Phylogeny; D020161:Physical Chromosome Mapping; D013045:Species Specificity
chemical_list: D005656:Fungal Proteins
keywords: Amanita; carbohydrate metabolism; comparative genomics; evolution of symbiosis; evolutionary novelty; horizontal gene transfer (HGT); saprotrophy