BACKGROUND: Termites primarily feed on lignocellulose or soil in association with specific gut microbes. The functioning of the termite gut microbiota is partly understood in a handful of wood-feeding pest species but remains largely unknown in other taxa. We intend to fill this gap and provide a global understanding of the functional evolution of termite gut microbiota. RESULTS: We sequenced the gut metagenomes of 145 samples representative of the termite diversity. We show that the prokaryotic fraction of the gut microbiota of all termites possesses similar genes for carbohydrate and nitrogen metabolisms, in proportions varying with termite phylogenetic position and diet. The presence of a conserved set of gut prokaryotic genes implies that essential nutritional functions were present in the ancestor of modern termites. Furthermore, the abundance of these genes largely correlated with the host phylogeny. Finally, we found that the adaptation to a diet of soil by some termite lineages was accompanied by a change in the stoichiometry of genes involved in important nutritional functions rather than by the acquisition of new genes and pathways. CONCLUSIONS: Our results reveal that the composition and function of termite gut prokaryotic communities have been remarkably conserved since termites first appeared ~ 150 million years ago. Therefore, the "world's smallest bioreactor" has been operating as a multipartite symbiosis composed of termites, archaea, bacteria, and cellulolytic flagellates since its inception. Video Abstract.

Division of Forest Science Kangwon National University Chuncheon Republic of Korea

Evolutionary Biology and Ecology Université Libre de Bruxelles Brussels Belgium

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

Faculty of Tropical AgriSciences Czech University of Life Sciences Prague Czech Republic

Okinawa Institute of Science and Technology Graduate University 1919 1 Tancha Onna son Okinawa 904 0495 Japan

Research Group Insect Gut Microbiology and Symbiosis Max Planck Institute for Terrestrial Microbiology Marburg Germany

School of Life and Environmental Sciences University of Sydney Sydney NSW 2006 Australia

Tropical Biosphere Research Center Center of Molecular Biosciences University of the Ryukyus Nishihara Okinawa 903 0213 Japan

University Sorbonne Paris Nord Laboratory of Experimental and Comparative Ethology LEEC UR 4443 Villetaneuse France

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