Animals harbor specialized bacterial communities in their guts referred to as gut microbiota. These communities are typically composed of hundreds of different species. Moreover, most of these species are composed of a multitude of divergent strains. Despite recent advances in understanding the functional importance of the gut microbiota for host health, surprisingly little is known about the distribution of closely related strains across hosts, their genomic diversity, evolutionary dynamics, or functional relevance. The complex nature of microbial communities and the fact that diversity is typically assessed using marker gene analyses, instead of genomic approaches, have precluded a detailed understanding of how strain-level diversity is generated and maintained neither in the gut microbiota nor in any other natural microbial community.
MicroBeeOme addressed these questions by studying the gut microbiome of honey bees. Previous research has shown that the dominant bacterial lineages of the honey bee gut microbiota have substantially diversified. Moreover, gnotobiotic bee systems have been established that allow to colonize microbiota-free bees with defined communities composed of cultured strains. This provided us with a unique opportunities to study microbial ecology and evolution in the animal gut in a simple and experimentally amenable system. The project was divided into four work packages addressing interconnected research questions of current biology: (i) Determining the population genomic structure of closely related gut bacteria, (ii) investigating how closely related gut bacteria interact with each other, (iii) elucidating the underlying genetic and molecular mechanisms, and (iv) revealing their impact on the symbiosis with the host. To this end, we applied a multidisciplinary approach combining comparative metagenomics, transcriptomics, metabolomics, gnotobiotic bee experiments, microscopy, bacterial genetics, and automated bee tracking. In summary, the project has revealed how diversity at the level of strains is structured and distributed across bee species, colonies, and individual bees. We have identified that closely related strains engage in negative interactions in the bee gut, yet can stably coexist in the presence of the right diet, and identified gene sets involved in symbiotic interactions in the gut. Finally, we have found that the bee gut microbiota increases the head-to-head interactions among bees in a colony, demonstrating the critical role of these bacteria for the social lifestyle of these important pollinator species. These findings advance our understanding of the ecology and evolution of strain-level diversity in microbiomes and provide novel insights into the interaction between honey bees with their gut bacteria.
