Preface The gut microbiota can have profound effects on hosts, but studying these relationships in humans presents challenges. The specialized gut community of honey bees parallels the mammalian microbiota, as both are mostly composed of host-adapted, facultative anaerobes and microaerophiles. The bee gut community, however, is far simpler, being dominated by only nine bacterial species clusters that are only associated with bees and that are transmitted through social interactions between individuals. Recent developments, including the discovery of extensive strain-level variation, evidence of protective and nutritional functions, and reports of eco-physiological or disease-associated community perturbations, have drawn attention to the microbiota’s role in bee health, as well as its potential as a model for studying gut symbiont ecology and evolution.

Honey bees, bumble bees, and stingless bees have related gut microbial communities that are shaped by host evolutionary history.

Gilliamella apicola and Snodgrassella alvi are dominant members of the honey bee (Apis spp.) and bumble bee (Bombus spp.) gut microbiota. We generated complete genomes of the type strains G. apicola wkB1 T and S. alvi wkB2 T (isolated from Apis), as well as draft genomes for four other strains from Bombus. G. apicola and S. alvi were found to occupy very different metabolic niches: The former is a saccharolytic fermenter, whereas the latter is an oxidizer of carboxylic acids. Together, they may form a syntrophic network for partitioning of metabolic resources. Both species possessed numerous genes [type 6 secretion systems, repeats in toxin (RTX) toxins, RHS proteins, adhesins, and type IV pili] that likely mediate cell-cell interactions and gut colonization. Variation in these genes could account for the host fidelity of strains observed in previous phylogenetic studies. Here, we also show the first experimental evidence, to our knowledge, for this specificity in vivo: Strains of S. alvi were able to colonize their native bee host but not bees of another genus. Consistent with specific, long-term host association, comparative genomic analysis revealed a deep divergence and little or no gene flow between Apis and Bombus gut symbionts. However, within a host type (Apis or Bombus), we detected signs of horizontal gene transfer between G. apicola and S. alvi, demonstrating the importance of the broader gut community in shaping the evolution of any one member. Our results show that host specificity is likely driven by multiple factors, including direct host-microbe interactions, microbe-microbe interactions, and social transmission.bacterial genomics | strain variation | symbiosis H ost specialization is a key evolutionary process in many symbionts. For bacteria, closely related strains of the same species may carry unique gene assemblages favoring the colonization of certain host species over others. The genetic basis of host specificity has been of considerable interest in the study of pathogens, but only a few studies of this process are available for mutualistic symbionts, including the normal gut microbiota (1-3). Despite tremendous advances in this field, most comparative studies of gut microbes rely on metagenomic and 16S rRNA gene surveys that typically give very coarse-grained information about evolutionary processes at the subspecies level. Modeling the differentiation of individual strains and discerning the factors that drive their specialization require both complete genome sequences and tractable systems with which to test hypotheses.In vertebrates, a well-recognized example of strain-level diversification is with Lactobacillus reuteri, a highly host-specific gut microbe found in diverse mammals and birds, for which multiple genome sequences and mouse-model approaches are available (4, 5). L. reuteri strains not only carry unique genes that restrict host colonization but also exhibit different patterns of genomic evolution according to their preferred host (6). Congruence between host phylogeny and bac...