Genomic changes underlying host specialization in the bee gut symbiont Lactobacillus Firm5

Abstract

Bacteria that engage in long-standing associations with particular hosts are expected to evolve host-specific adaptations that limit their capacity to thrive in other environments. Consistent with this, many gut symbionts seem to have a limited host range, based on community profiling and phylogenomics. However, few studies have experimentally investigated host specialization of gut symbionts and the underlying mechanisms have largely remained elusive. Here, we studied host specialization of a dominant gut symbiont of social bees, Lactobacillus Firm5. We show that Firm5 strains isolated from honey bees and bumble bees separate into deep-branching host-specific phylogenetic lineages. Despite their divergent evolution, colonization experiments show that bumble bee strains are capable of colonizing the honey bee gut. However, they were less successful than honey bee strains, and competition with honey bee strains completely abolished their colonization. In contrast, honey bee strains of divergent phylogenetic lineages were able to coexist within individual bees. This suggests that both host selection and interbacterial competition play important roles in host specialization. Using comparative genomics of 27 Firm5 isolates, we found that the genomes of honey bee strains harbour more carbohydrate-related functions than bumble bee strains, possibly providing a competitive advantage in the honey bee gut. Remarkably, most of the genes encoding carbohydrate-related functions were not conserved among the honey bee strains, which suggests that honey bees can support a metabolically more diverse community of Firm5 strains than bumble bees. These findings advance our understanding of the genomic changes underlying host specialization.

Cadmium and Selenate Exposure Affects the Honey Bee Microbiome and Metabolome, and Bee-Associated Bacteria Show Potential for Bioaccumulation

“…We used RAST annotations of publicly available honey bee gut bacterial genomes to search for putative mechanisms for toxicant tolerance or sensitivity, although we note that automatic genome annotations do not necessarily correspond to the correct function of each gene. We show that genes corresponding to cadmium resistance and selenium transport are common in the bee gut microbiome, and, as bee symbionts have functionally diverse genomes (78)(79)(80)(81)(82)(83), strain-level variation may explain the differences in treatment response between individual ESVs of bacteria corresponding to the same phylotype. Furthermore, putative toxicant resistance genes may not predict symbiont response to toxicants in the dynamic environment of the bee gut, within which diverse host/microbe interactions occur (84).…”

Honey bees harbor a diverse gut virome engaging in nested strain-level interactions with the microbiota

“…The bee gut microbiota is comprised of only 8 to 10 bacterial phylotypes (i.e., 16S rRNA sequences that cluster at >97%), most of which contain several divergent lineages and a high extent of strain-level diversity (33)(34)(35). All bacterial phylotypes can be cultured in the laboratory and microbiotadepleted bees can be colonized with defined communities of cultured strains (36)(37)(38)(39). This allows us to disentangle roles of individual community members which contributes to our fundamental understanding of how microbiomes function.…”

Microbial Diversity Associated with the Pollen Stores of Captive-Bred Bumble Bee Colonies

“…Bumble bee colonies are founded by a single overwintered queen, and only the microbes colonizing the queen are expected to be transferred to the residents of the newly initiated colony. The single-queen generational inheritance can cause severe transmission bottlenecks, leading to a loss in microbial diversity and emergent function [30,85,86]. Commercial colonies, which have fewer opportunities to acquire microbes from their foraging environment, may be more vulnerable to such losses in microbial diversity.…”