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

Abstract

23Bacteria that engage in longstanding associations with particular hosts are expected 24 to evolve host-specific adaptations that limit their capacity to thrive in other 25 environments. Consistent with this, many gut symbionts seem to have a limited host 26 range, based on community profiling and phylogenomics. However, few studies have 27 experimentally investigated host specialization of gut symbionts and underlying 28 mechanisms have largely remained elusive. Here, we studied host specialization of a 29 dominant gut symbiont of social bees, Lactobacillus Firm5. We show that Firm5 30 strains isolated from honey bees and bumble bees separate into deep-branching host-31 specific phylogenetic lineages. Despite their divergent evolution, colonization 32 experiments show that bumble bee strains are capable of colonizing the honey bee 33 gut. However, they were less successful than honey bee strains, and competition with 34 honey bee strains completely abolished their colonization. In contrast honey bee 35 strains of divergent phylogenetic lineages were able to coexist within individual bees. 36This suggests that both host selection and interbacterial competition play important 37 roles for host specialization. Using comparative genomics of 27 Firm5 isolates, we 38 found that the genomes of honey bee strains harbor more carbohydrate-related 39 functions than bumble bee strains, possibly providing a competitive advantage in the 40 honey bee gut. Remarkably, most of the genes encoding carbohydrate-related 41 functions were not conserved among the honey bee strains, which suggests that 42 honey bees can support a metabolically more diverse community of Firm5 strains 43 than bumble bees. These findings advance our understanding of genomic changes 44 underlying host specialization. 45

Division of labor in honey bee gut microbiota for plant polysaccharide digestion

“…S1A), corroborating previous findings (22). Further, strains from Apis hosts generally cluster separately from those from Bombus hosts, as found for other bee gut bacteria (23,24). Bifidobacterium from Bombus are derived from 2 distinct phylogenetic lineages.…”

“…GHs involved in pectin hydrolysis were also identified in other genera of bee gut bacteria, in particular, some Lactobacillus and Bifidobacterium species possess GH5, GH78, and GH28 genes (Fig. 1 and Dataset S2), although the occurrence of GH genes is limited and highly variable among Lactobacillus strains (24). Thus, degradation of pectin including extensive glycosyl side chains requires a diverse array of enzymes (40); collaborative actions of both PLs (PL1, PL9, PL22) and GHs (GH43, GH5, GH78, GH28) might be required for degradation of pectin in the bee gut (16).…”

Niche partitioning facilitates coexistence of closely related gut bacteria

“…This is consistent with previous observations that negative interactions predominate in nutrient-rich environments 31,34–37 , such as the animal gut or culture media. In addition, the studied Lactobacillus species are likely to have similar nutritional requirements 38–40 , as they harbor relatively small genomes (1.5-2Mb) with a conserved and streamlined core metabolism and overlapping auxotrophies.…”

“…It has previously been speculated that the large diversity of carbohydrate transport and metabolism functions in the accessory gene pool of Lactobacillus is an adaptation to the pollen-based diet of the host and a consequence of the nutrient competition with closely related species 22,38 . Our findings support this hypothesis and provide first experimental evidence for the link between the coexistence of diverse Lactobacilli species in the honey bee gut, the large diversity of carbohydrate metabolism related functions in their genomes, and the pollen diet of the host.…”

“…This is consistent with previous observations that negative interactions predominate in nutrient-rich environments 31, 34–37 . Moreover, the four Lactobacillus species harbor relatively small genomes (1.5-2Mb) with a conserved and streamlined core metabolism and similar auxotrophies, suggesting overlapping nutritional requirements 38–40 .…”