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

Research output: Contribution to journalJournal articleResearchpeer-review

Michael Thomas-Poulsen, Haofu Hu, Cai Li, Zhensheng Chen, Luohao Xu, Saria Otani, Sanne Nygaard, Tania Nobre, Sylvia Klaubauf, Philipp M Schindler, Frank Hauser, Hailin Pan, Zhikai Yang, Anton S.M. Sonnenberg, Z. Wilhelm de Beer, Yong Zhang, Michael J Wingfield, Cornelis Grimmelikhuijzen, Ronald P. de Vries, Judith Korb & 4 others Duur K. Aanen, Jun Wang, Jacobus Jan Boomsma, Guojie Zhang

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.

Original languageEnglish
Article number14500-14505
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number40
Number of pages6
ISSN0027-8424
DOIs
Publication statusPublished - 2014

ID: 124167649