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

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

    Research output: Contribution to journal/periodicalArticleScientificpeer-review

    195 Citations (Scopus)

    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.

    Original languageEnglish
    Pages (from-to)14500-14505
    Number of pages6
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume111
    Issue number40
    DOIs
    Publication statusPublished - 07 Oct 2014

    Keywords

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

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