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 - 2014/10/7
Y1 - 2014/10/7
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
SN - 0027-8424
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
IS - 40
M1 - 14500-14505
ER -