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.carbohydrate-active enzymes | eusocial | symbioses | cellulose | lignin

Lignocellulose pretreatment in a fungus-cultivating termite

“…Attempts to identify these compounds were not successful (details provided in SI Appendix, SI Materials and Methods). Consistent with previous reports that Termitomyces fungi are genetically enriched in polysaccharide backbone-degrading enzymes and depleted in oligosaccharidesplitting enzymes (9,16), our results demonstrate that the funguscomb microbiome contributes to significant polysaccharide cleavage/ depolymerization, leaving the mature comb enriched in oligosaccharides, particularly cellulosic oligomers/polymers.…”

“…1 A and B) (8). Throughout their evolutionary history, fungus-cultivating termites have evolved in mutualistic association with multiple microbial symbionts, not only with the lignocellulose-digesting basidiomycete fungi Termitomyces spp., but also with gut microbiota and the bacterial community associated with their fungus comb (8,9). The Macrotermitinae termite-fungus-bacterial symbiosis is a system that enables the extensive conversion of plant materials (9,10).…”

“…Throughout their evolutionary history, fungus-cultivating termites have evolved in mutualistic association with multiple microbial symbionts, not only with the lignocellulose-digesting basidiomycete fungi Termitomyces spp., but also with gut microbiota and the bacterial community associated with their fungus comb (8,9). The Macrotermitinae termite-fungus-bacterial symbiosis is a system that enables the extensive conversion of plant materials (9,10). In addition, the plant substrate processing in fungus-cultivating termites is completed by the termite worker castes with complex age-related labor division (genera Odontotermes and Macrotermes) (11,12) (Fig.…”

Hemimetabolous genomes reveal molecular basis of termite eusociality

“…The cockroach genome (2.0 Gb) is considerably larger than all three termite genomes. The genome size of C. secundus (1.30 Gb) is comparable to the higher, fungus-growing termite Macrotermes natalensis (1.31 Gb, Termitidae) 16 , but more than twice as large as the lower, dampwood termite Zootermopsis nevadensis (562 Mb, Termopsidae) 17 . The smaller genomes of termites compared to the cockroach are in line with previous size estimations based on C-values 18 .…”

Transitional Complexity of Social Insect Immunity

“…Indeed, recent studies have provided insights into the complimentary roles of innate immunity and gut microbiota. For example, bacteria with antimicrobial and fungal cell wall degradation properties are found to be present in termite gut and nest microbiotas Poulsen et al, 2014;Rosengaus et al, 2014) with higher abundances compared to their ancestral solitary cockroaches (Dietrich et al, 2014;Otani et al, 2014). In bees, a number of antimicrobial peptide-producing bacteria have been sequenced to show that they are selectively higher in abundance in bees compared to Drosophila (Wong et al, 2011 and references therein).…”