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
Fungus-growing ants engage in mutualistic associations with both the fungus they cultivate for food and actinobacteria (Pseudonocardia spp.) that produce selective antibiotics to defend that fungus from specialized fungal parasites. In the first system to be analyzed at the molecular level, the bacterium associated with the ant Apterostigma dentigerum produces dentigerumycin, a cyclic depsipeptide with highly modified amino acids, to selectively inhibit the parasitic fungus (Escovopsis sp.).
E usociality, the reproductive division of labour with overlapping generations and cooperative brood care, is one of the major evolutionary transitions in biology 1 . Although rare, eusociality has been observed in a diverse range of organisms, including shrimps, mole rats and several insect lineages [2][3][4] . A particularly striking case of convergent evolution occurred within the holometabolous Hymenoptera and in the hemimetabolous termites (Isoptera), which are separated by over 350 Myr of evolution 5 . Termites evolved within the cockroaches around 150 Myr ago, towards the end of the Jurassic period 6,7 , about 50 Myr before the first bees and ants appeared 5 . Therefore, identifying the molecular mechanisms common to both origins of eusociality is crucial to understanding the fundamental signatures of these rare evolutionary transitions. While the availability of genomes from many eusocial and non-eusocial hymenopteran species 8 has allowed extensive research into the origins of eusociality within ants and bees [9][10][11] , a paucity of genomic data from cockroaches and termites has precluded large-scale investigations into the evolution of eusociality in this hemimetabolous clade.The conditions under which eusociality arose differ greatly between the two groups. Termites and cockroaches are hemimetabolous and so show a direct development, while holometabolous hymenopterans complete the adult body plan during metamorphosis. In termites, workers are immatures and only reproductive castes are adults 12 , while in Hymenoptera, adult workers and queens represent the primary division of labour. Moreover, termites are diploid and their colonies consist of both male and female workers, and usually a queen and king dominate reproduction. This is in contrast to the haplodiploid system found in Hymenoptera, in which all workers and dominant reproductives are female. It is therefore intriguing that strong similarities have evolved convergently within the termites and the hymenopterans, such as differentiated castes and a nest life with reproductive division of labour. The termites can be subdivided into wood-dwelling and foraging termites. The former belong to the lower termites and produce simple, small colonies with totipotent workers that can become reproductives. Foraging termites (some lower and all higher termites) form large, complex societies, in which worker castes can be irreversible 12 . For this reason, higher, but not lower, termites can be classed as superorganismal 13 . Similarly, within Hymenoptera, varying levels of eusociality exist.Here we provide insights into the molecular signatures of eusociality within the termites. We analysed the genomes of two lower and one higher termite species and compared them to the genome
Attine ants engage in a quadripartite symbiosis with fungi they cultivate for food, specialized garden parasites, and parasite-inhibiting bacteria. Molecular phylogenetic evidence supports an ancient host-pathogen association between the ant-cultivar mutualism and the garden parasite. Here we show that ants rear the antibiotic-producing bacteria in elaborate cuticular crypts, supported by unique exocrine glands, and that these structures have been highly modified across the ants' evolutionary history. This specialized structural evolution, together with the absence of these bacteria and modifications in other ant genera that do not grow fungus, indicate that the bacteria have an ancient and coevolved association with the ants, their fungal cultivar, and the garden parasite.
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