Functional Metagenomics and Evolution of Termite Gut Microbiome

Termites are amongst the most abundant terrestrial animals on earth, primarily due to their ability to digest lignocellulose, the most abundant organic molecule. Lignocellulose is broken down in the termite gut with the help of symbiotic microbes, including protists, archaea, and bacteria. Studies using fragments of the 16S ribosomal RNA gene have shown that termites and their gut bacteria have had a complex coevolutionary history. In addition, the bacterial communities found in termite guts vary with termite diet. Up to now, studies have been focusing on termite species that are easy to sample or have a pest status. This sampling bias against early evolving termite lineages and lineages feeding on substrates other than wood preclude a global understanding of the evolutionary history of termites and their gut microbes. To fill this gap, I sequenced whole gut metagenomes of 201 termite samples and one sample of a species of Cryptocercus, the cockroach genus sister to termites. The samples were selected from across the termite tree of life and represent termite phylogenetic and dietary diversity. My thesis showcases that (i) the gut microbiome of all termites possess similar genes for carbohydrate breakdown and other metabolic pathways involved in the digestion of carbohydrates. The proportion of these genes vary with termite phylogeny and diet. Still, the acquisition of a soil diet from a wood-feeding ancestor was accompanied by changes in gene abundance rather than by the acquisition of new genes and pathways. Using ten single-copy protein-coding marker gene sequences, (ii) I studied the pattern of coevolution between termites and their gut bacteria. Significant cophylogenetic signals with termites were found for tens of gut bacterial lineages that were either acquired by the common ancestor of all termites or by specific termite lineages. Finally, (iii) I investigated the role of horizontal gene transfer on the acquisition of carbohydrate metabolizing gene families by the termite gut microbes. I found gene family-specific transfers from the environment and from bacteria belonging to lineages present in the termite gut, suggesting that horizontal gene transfer events are common among bacteria of termite guts. Overall, my Ph.D. thesis sheds new light on how the gut microbiome has coevolved with its termite hosts since the inception of this nutritional symbiosis, some 150 million years ago.Okinawa Institute of Science and Technology Graduate Universit