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Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14500-5. doi: 10.1073/pnas.1319718111. Epub 2014 Sep 22.

Complementary symbiont contributions to plant decomposition in a fungus-farming termite.

Author information

1
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark; mpoulsen@bio.ku.dk zhanggj@genomics.cn.
2
China National Genebank, BGI-Shenzen, Shenzhen 518083, China;
3
China National Genebank, BGI-Shenzen, Shenzhen 518083, China; Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen, Denmark;
4
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
5
Laboratory of Genetics, Wageningen University, 6708 PB, Wageningen, The Netherlands;
6
Fungal Biodiversity Centre, Centraalbureau voor Schimmelcultures, Royal Netherlands Academy of Arts and Sciences, NL-3584 CT, Utrecht, The Netherlands;
7
Behavioral Biology, Fachbereich Biology/Chemistry, University of Osnabrück, D-49076 Osnabrück, Germany;
8
Center for Functional and Comparative Insect Genomics, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark;
9
Department of Plant Breeding, Wageningen University and Research Centre, NL-6708 PB, Wageningen, The Netherlands;
10
Department of Microbiology, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Pretoria SA-0083, South Africa; and.
11
China National Genebank, BGI-Shenzen, Shenzhen 518083, China; Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark.
12
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.

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.

KEYWORDS:

carbohydrate-active enzymes; cellulose; eusocial; lignin; symbioses

PMID:
25246537
PMCID:
PMC4209977
DOI:
10.1073/pnas.1319718111
[Indexed for MEDLINE]
Free PMC Article

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