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

dc.contributor.authorPoulson, Michael
dc.contributor.authorHu, Haofu
dc.contributor.authorLi, Cai
dc.contributor.authorChen, Zhensheng
dc.contributor.authorXu, Luohao
dc.contributor.authorOtani, Saria
dc.contributor.authorNygaard, Sanne
dc.contributor.authorNobre, Tania
dc.contributor.authorKlaubauf, Sylvia
dc.contributor.authorSchindler, Philipp M.
dc.contributor.authorHauser, Frank
dc.contributor.authorPan, Hailin
dc.contributor.authorYang, Zhikai
dc.contributor.authorSonnenberg, Anton S.M.
dc.contributor.authorDe Beer, Z. Wilhelm
dc.contributor.authorZhang, Yong
dc.contributor.authorWingfield, Michael J.
dc.contributor.authorGrimmelikhuijzen, Cornelis J.P.
dc.contributor.authorDe Vries, Ronald P.
dc.contributor.authorKorb, Judith
dc.contributor.authorAanen, Duur K.
dc.contributor.authorWang, Jun
dc.contributor.authorBoomsma, Jacobus J.
dc.contributor.authorZhang, Guojie
dc.date.accessioned2014-11-17T12:07:57Z
dc.date.available2014-11-17T12:07:57Z
dc.date.issued2014
dc.description.abstractTermites 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.en_US
dc.description.librarianhj2014en_US
dc.description.sponsorshipA STENO grant from The Danish Council for Independent Research | Natural Sciences (to M.P.), Danish National Research Foundation Centre of Excellence Grant DNRF57 (to J.J.B.), and a Marie Curie International Incoming Fellowship (300837; to G.Z.).en_US
dc.description.urihttp://www.pnas.org/en_US
dc.identifier.citationPoulson, M, Hu, H, Li, C, Chen, Z, Xu, L, Otani, S, Nygaard, S, Nobre, T, Klaubauf, S, Schindler, PM, Hauser, F, Pan, H, Yang, Z, Sonnenberg, ASM, De Beer, ZW, Zhang, Y, Wingfield, MJ, Grimmelikhuijzen, CJP, De Vries, RP, Korb, J, Aanen, DK, Wang, J, Boomsma, JJ & Zhang, G 2014, 'Complementary symbiont contributions to plant decomposition in a fungus-farming termite', Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 40, pp. 14500-14505.en_US
dc.identifier.issn0027-8424 (print)
dc.identifier.issn1091-6490 (online)
dc.identifier.other10.1073/pnas.1319718111
dc.identifier.urihttp://hdl.handle.net/2263/42642
dc.language.isoenen_US
dc.publisherNational Academy of Sciencesen_US
dc.rights© 2014 by the National Academy of Sciencesen_US
dc.subjectCarbohydrate-active enzymesen_US
dc.subjectEusocialen_US
dc.subjectSymbiosesen_US
dc.subjectCelluloseen_US
dc.subjectLigninen_US
dc.titleComplementary symbiont contributions to plant decomposition in a fungus-farming termiteen_US
dc.typePostprint Articleen_US

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