title: Complementary symbiont contributions to plant decomposition in a fungus-farming termite.
abstract: Termites normally rely on gut symbionts to decompose organic matter but the Macrotermitinae domesticated Termitomyces fungi to produce their own food. This transition was accompanied by a shift in the composition of the gut microbiota, but the complementary roles of these bacteria in the symbiosis have remained enigmatic. We obtained high-quality annotated draft genomes of the termite Macrotermes natalensis, its Termitomyces symbiont, and gut metagenomes from workers, soldiers, and a queen. We show that members from 111 of the 128 known glycoside hydrolase families are represented in the symbiosis, that Termitomyces has the genomic capacity to handle complex carbohydrates, and that worker gut microbes primarily contribute enzymes for final digestion of oligosaccharides. This apparent division of labor is consistent with the Macrotermes gut microbes being most important during the second passage of comb material through the termite gut, after a first gut passage where the crude plant substrate is inoculated with Termitomyces asexual spores so that initial fungal growth and polysaccharide decomposition can proceed with high efficiency. Complex conversion of biomass in termite mounds thus appears to be mainly accomplished by complementary cooperation between a domesticated fungal monoculture and a specialized bacterial community. In sharp contrast, the gut microbiota of the queen had highly reduced plant decomposition potential, suggesting that mature reproductives digest fungal material provided by workers rather than plant substrate.
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark; mpoulsen@bio.ku.dk zhanggj@genomics.cn.
authors.forename: Michael
authors.identifier: http://orcid.org/0000-0002-2839-1715
authors.initials: M
authors.lastname: Poulsen
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China;
authors.forename: Haofu
authors.initials: H
authors.lastname: Hu
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China; Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen, Denmark;
authors.forename: Cai
authors.initials: C
authors.lastname: Li
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China;
authors.forename: Zhensheng
authors.initials: Z
authors.lastname: Chen
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China;
authors.forename: Luohao
authors.identifier: http://orcid.org/0000-0002-3714-8047
authors.initials: L
authors.lastname: Xu
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
authors.forename: Saria
authors.initials: S
authors.lastname: Otani
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
authors.forename: Sanne
authors.initials: S
authors.lastname: Nygaard
authors.affiliation: Laboratory of Genetics, Wageningen University, 6708 PB, Wageningen, The Netherlands;
authors.forename: Tania
authors.initials: T
authors.lastname: Nobre
authors.affiliation: Fungal Biodiversity Centre, Centraalbureau voor Schimmelcultures, Royal Netherlands Academy of Arts and Sciences, NL-3584 CT, Utrecht, The Netherlands;
authors.forename: Sylvia
authors.initials: S
authors.lastname: Klaubauf
authors.affiliation: Behavioral Biology, Fachbereich Biology/Chemistry, University of Osnabrück, D-49076 Osnabrück, Germany;
authors.forename: Philipp M
authors.initials: PM
authors.lastname: Schindler
authors.affiliation: Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
authors.forename: Frank
authors.initials: F
authors.lastname: Hauser
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China;
authors.forename: Hailin
authors.initials: H
authors.lastname: Pan
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China;
authors.forename: Zhikai
authors.initials: Z
authors.lastname: Yang
authors.affiliation: Department of Plant Breeding, Wageningen University and Research Centre, NL-6708 PB, Wageningen, The Netherlands;
authors.forename: Anton S M
authors.initials: AS
authors.lastname: Sonnenberg
authors.affiliation: Department of Microbiology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria SA-0083, South Africa; and.
authors.forename: Z Wilhelm
authors.initials: ZW
authors.lastname: de Beer
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China;
authors.forename: Yong
authors.initials: Y
authors.lastname: Zhang
authors.affiliation: Department of Microbiology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria SA-0083, South Africa; and.
authors.forename: Michael J
authors.initials: MJ
authors.lastname: Wingfield
authors.affiliation: Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
authors.forename: Cornelis J P
authors.initials: CJ
authors.lastname: Grimmelikhuijzen
authors.affiliation: Fungal Biodiversity Centre, Centraalbureau voor Schimmelcultures, Royal Netherlands Academy of Arts and Sciences, NL-3584 CT, Utrecht, The Netherlands;
authors.forename: Ronald P
authors.initials: RP
authors.lastname: de Vries
authors.affiliation: Behavioral Biology, Fachbereich Biology/Chemistry, University of Osnabrück, D-49076 Osnabrück, Germany;
authors.forename: Judith
authors.initials: J
authors.lastname: Korb
authors.affiliation: Laboratory of Genetics, Wageningen University, 6708 PB, Wageningen, The Netherlands;
authors.forename: Duur K
authors.initials: DK
authors.lastname: Aanen
authors.affiliation: China National Genebank, BGI-Shenzen, Shenzhen 518083, China; Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark.
authors.forename: Jun
authors.initials: J
authors.lastname: Wang
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
authors.forename: Jacobus J
authors.initials: JJ
authors.lastname: Boomsma
authors.affiliation: Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark; China National Genebank, BGI-Shenzen, Shenzhen 518083, China; mpoulsen@bio.ku.dk zhanggj@genomics.cn.
authors.forename: Guojie
authors.initials: G
authors.lastname: Zhang
mesh_terms: D000818:Animals; D001419:Bacteria / Q000145:classification / Q000235:genetics / Q000378:metabolism; D050260:Carbohydrate Metabolism; D004064:Digestive System / Q000378:metabolism / Q000382:microbiology; D005260:Female; D005656:Fungal Proteins / Q000378:metabolism; D006026:Glycoside Hydrolases / Q000378:metabolism; D054884:Host-Pathogen Interactions; D020049:Isoptera / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology; D008297:Male; D054892:Metagenome / Q000235:genetics; D059013:Microbial Consortia / Q000235:genetics / Q000502:physiology; D009844:Oligosaccharides / Q000378:metabolism; D010944:Plants / Q000378:metabolism*; D011134:Polysaccharides / Q000378:metabolism; D017422:Sequence Analysis, DNA; D013559:Symbiosis; D055434:Termitomyces / Q000235:genetics / Q000378:metabolism* / Q000502:physiology
chemical_list: D005656:Fungal Proteins; D009844:Oligosaccharides; D011134:Polysaccharides; D006026:Glycoside Hydrolases
keywords: carbohydrate-active enzymes; cellulose; eusocial; lignin; symbioses