The gut microbiota of animals exert major effects on host biology [1]. Although horizontal transfer is generally considered the prevalent route for the acquisition of gut bacteria in mammals [2], some bacterial lineages have co-speciated with their hosts on timescales of several million years [3]. Termites harbor a complex gut microbiota, and their advanced social behavior provides the potential for long-term vertical symbiont transmission, and co-evolution of gut symbionts and host [4-6]. Despite clear evolutionary patterns in the gut microbiota of termites [7], a consensus on how microbial communities were assembled during termite diversification has yet to be reached. Although some studies have concluded that vertical transmission has played a major role [8, 9], others indicate that diet and gut microenvironment have been the primary determinants shaping microbial communities in termite guts [7, 10]. To address this issue, we examined the gut microbiota of 94 termite species, through 16S rRNA metabarcoding. We analyzed the phylogeny of 211 bacterial lineages obtained from termite guts, including their closest relatives from other environments, which were identified using BLAST. The results provided strong evidence for rampant horizontal transfer of gut bacteria between termite host lineages. Although the majority of termite-derived phylotypes formed large monophyletic groups, indicating high levels of niche specialization, numerous other clades were interspersed with bacterial lineages from the guts of other animals. Our results indicate that "mixed-mode" transmission, which combines colony-to-offspring vertical transmission with horizontal colony-to-colony transfer, has been the primary driving force shaping the gut microbiota of termites.

Department of Biogeochemistry Max Planck Institute for Terrestrial Microbiology Marburg Germany

Department of Biogeochemistry Max Planck Institute for Terrestrial Microbiology Marburg Germany; Strategy and Innovation Technology Center Siemens Healthcare Erlangen Germany

Department of Biological Sciences National University of Singapore 117543 Singapore Singapore

Department of Biological Sciences National University of Singapore 117543 Singapore Singapore; School of Animal Biology University of Western Australia Perth WA 6009 Australia

Evolutionary Biology and Ecology Université Libre de Bruxelles Bruxelles Belgium

Faculty of Forestry and Wood Sciences 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; School of Life and Environmental Sciences University of Sydney Sydney NSW 2006 Australia; Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Czech Republic

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

Comment In

Trends Microbiol. 2018 Jul;26(7):557-559. doi: 10.1016/j.tim.2018.04.005. PubMed

References provided by Crossref.org

Metabolic diversity and responses of anteater clostridial isolates to chitin-based substrates

Termites and subsocial roaches inherited many bacterial-borne carbohydrate-active enzymes (CAZymes) from their common ancestor

Genome reduction and horizontal gene transfer in the evolution of Endomicrobia-rise and fall of an intracellular symbiosis with termite gut flagellates

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Evidence of cospeciation between termites and their gut bacteria on a geological time scale

The functional evolution of termite gut microbiota

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Termites Are Associated with External Species-Specific Bacterial Communities

Unmapped RNA Virus Diversity in Termites and their Symbionts

Phylogenomic analysis of 589 metagenome-assembled genomes encompassing all major prokaryotic lineages from the gut of higher termites