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

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

Complementary symbiont contributions to plant decomposition in a fungus-farming termite. / Thomas-Poulsen, Michael; Hu, Haofu; Li, Cai; Chen, Zhensheng; Xu, Luohao; Otani, Saria; Nygaard, Sanne; Nobre, Tania; Klaubauf, Sylvia; Schindler, Philipp M; Hauser, Frank; Pan, Hailin; Yang, Zhikai; Sonnenberg, Anton S.M.; de Beer, Z. Wilhelm; Zhang, Yong; Wingfield, Michael J; Grimmelikhuijzen, Cornelis; de Vries, Ronald P.; Korb, Judith; Aanen, Duur K.; Wang, Jun; Boomsma, Jacobus Jan; Zhang, Guojie.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 40, 14500-14505, 2014.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Thomas-Poulsen, 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, C, 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, 14500-14505. https://doi.org/10.1073/pnas.1319718111

APA

Thomas-Poulsen, M., Hu, H., Li, C., Chen, Z., Xu, L., Otani, S., Nygaard, S., Nobre, T., Klaubauf, S., Schindler, P. M., Hauser, F., Pan, H., Yang, Z., Sonnenberg, A. S. M., de Beer, Z. W., Zhang, Y., Wingfield, M. J., Grimmelikhuijzen, C., de Vries, R. P., ... 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, 111(40), [14500-14505]. https://doi.org/10.1073/pnas.1319718111

Vancouver

Thomas-Poulsen M, Hu H, Li C, Chen Z, Xu L, Otani S et al. Complementary symbiont contributions to plant decomposition in a fungus-farming termite. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(40). 14500-14505. https://doi.org/10.1073/pnas.1319718111

Author

Thomas-Poulsen, Michael ; Hu, Haofu ; Li, Cai ; Chen, Zhensheng ; Xu, Luohao ; Otani, Saria ; Nygaard, Sanne ; Nobre, Tania ; Klaubauf, Sylvia ; Schindler, Philipp M ; Hauser, Frank ; Pan, Hailin ; Yang, Zhikai ; Sonnenberg, Anton S.M. ; de Beer, Z. Wilhelm ; Zhang, Yong ; Wingfield, Michael J ; Grimmelikhuijzen, Cornelis ; de Vries, Ronald P. ; Korb, Judith ; Aanen, Duur K. ; Wang, Jun ; Boomsma, Jacobus Jan ; Zhang, Guojie. / Complementary symbiont contributions to plant decomposition in a fungus-farming termite. In: Proceedings of the National Academy of Sciences of the United States of America. 2014 ; Vol. 111, No. 40.

Bibtex

@article{e080588b74d24ef3a08ceb689c81169a,
title = "Complementary symbiont contributions to plant decomposition in a fungus-farming termite",
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.",
author = "Michael Thomas-Poulsen and Haofu Hu and Cai Li and Zhensheng Chen and Luohao Xu and Saria Otani and Sanne Nygaard and Tania Nobre and Sylvia Klaubauf and Schindler, {Philipp M} and Frank Hauser and Hailin Pan and Zhikai Yang and Sonnenberg, {Anton S.M.} and {de Beer}, {Z. Wilhelm} and Yong Zhang and Wingfield, {Michael J} and Cornelis Grimmelikhuijzen and {de Vries}, {Ronald P.} and Judith Korb and Aanen, {Duur K.} and Jun Wang and Boomsma, {Jacobus Jan} and Guojie Zhang",
year = "2014",
doi = "10.1073/pnas.1319718111",
language = "English",
volume = "111",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
publisher = "The National Academy of Sciences of the United States of America",
number = "40",

}

RIS

TY - JOUR

T1 - Complementary symbiont contributions to plant decomposition in a fungus-farming termite

AU - Thomas-Poulsen, Michael

AU - Hu, Haofu

AU - Li, Cai

AU - Chen, Zhensheng

AU - Xu, Luohao

AU - Otani, Saria

AU - Nygaard, Sanne

AU - Nobre, Tania

AU - Klaubauf, Sylvia

AU - Schindler, Philipp M

AU - Hauser, Frank

AU - Pan, Hailin

AU - Yang, Zhikai

AU - Sonnenberg, Anton S.M.

AU - de Beer, Z. Wilhelm

AU - Zhang, Yong

AU - Wingfield, Michael J

AU - Grimmelikhuijzen, Cornelis

AU - de Vries, Ronald P.

AU - Korb, Judith

AU - Aanen, Duur K.

AU - Wang, Jun

AU - Boomsma, Jacobus Jan

AU - Zhang, Guojie

PY - 2014

Y1 - 2014

N2 - 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.

AB - 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.

U2 - 10.1073/pnas.1319718111

DO - 10.1073/pnas.1319718111

M3 - Journal article

C2 - 25246537

VL - 111

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 40

M1 - 14500-14505

ER -

ID: 124167649