4.8 Article

The functional evolution of termite gut microbiota

Journal

MICROBIOME
Volume 10, Issue 1, Pages -

Publisher

BMC
DOI: 10.1186/s40168-022-01258-3

Keywords

Isoptera; Endosymbionts; Metagenomics; Vertical inheritance

Categories

Funding

  1. Czech Science Foundation [20-20548S]
  2. Internal Grant Agency of the Faculty of Tropical AgriSciences, CULS [20213112]
  3. Australian Research Council
  4. Japan Society for the Promotion of Science through a Kakenhi [17H01510]
  5. DC2 graduate student fellowship
  6. Grants-in-Aid for Scientific Research [17H01510] Funding Source: KAKEN

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By sequencing the gut metagenomes of 145 termite samples, the study reveals that the composition and function of termite gut microbiota have been remarkably conserved since the appearance of termites approximately 150 million years ago. This multipartite symbiosis, composed of termites, archaea, bacteria, and cellulolytic flagellates, has been functioning as the world's smallest bioreactor since its inception.
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 similar to 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.

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