Thomas-Poulsen, Michael11; Hu, Haofu5; Li, Cai12; Chen, Zhensheng5; Xu, Luohao5; Otani, Saria11; Nygaard, Sanne11; Nobre, Tania6; Klaubauf, Sylvia7; Schindler, Philipp M8; Hauser, Frank13; Pan, Hailin9; Yang, Zhikai9; Sonnenberg, Anton S.M.6; de Beer, Z. Wilhelm14; Zhang, Yong9; Wingfield, Michael J14; Grimmelikhuijzen, Cornelis13; de Vries, Ronald P.7; Korb, Judith8; Aanen, Duur K.6; Wang, Jun15; Boomsma, Jacobus Jan11; Zhang, Guojie11
1 Ecology and Evolution, Department of Biology, Faculty of Science, Københavns Universitet2 Natural History Museum of Denmark, Natural History Museum of Denmark, Faculty of Science, Københavns Universitet3 Cell Biology and Neurobiology, Department of Biology, Faculty of Science, Københavns Universitet4 Genome Research and Molecular Bio Medicine, Department of Biology, Faculty of Science, Københavns Universitet5 BGI-Shenzhen6 Wageningen University and Research Centre7 Royal Netherlands Academy of Arts and Sciences8 University of Osnabrück9 BGI-Shenzen10 University of Pretoria11 Ecology and Evolution, Department of Biology, Faculty of Science, Københavns Universitet12 Natural History Museum of Denmark, Natural History Museum of Denmark, Faculty of Science, Københavns Universitet13 Cell Biology and Neurobiology, Department of Biology, Faculty of Science, Københavns Universitet14 University of Pretoria15 Genome Research and Molecular Bio Medicine, Department of Biology, Faculty of Science, Københavns Universitet
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.
Proceedings of the National Academy of Sciences of the United States of America, 2014, Vol 111, Issue 40