Social bees harbor a simple and specialized microbiota that is spatially organized into different gut compartments. Recent results on the potential involvement of bee gut communities in pathogen protection and nutritional function have drawn attention to the impact of the microbiota on bee health. However, the contributions of gut microbiota to host physiology have yet to be investigated. Here we show that the gut microbiota promotes weight gain of both whole body and the gut in individual honey bees. This effect is likely mediated by changes in host vitellogenin, insulin signaling, and gustatory response. We found that microbial metabolism markedly reduces gut pH and redox potential through the production of short-chain fatty acids and that the bacteria adjacent to the gut wall form an oxygen gradient within the intestine. The short-chain fatty acid profile contributed by dominant gut species was confirmed in vitro. Furthermore, metabolomic analyses revealed that the gut community has striking impacts on the metabolic profiles of the gut compartments and the hemolymph, suggesting that gut bacteria degrade plant polymers from pollen and that the resulting metabolites contribute to host nutrition. Our results demonstrate how microbial metabolism affects bee growth, hormonal signaling, behavior, and gut physicochemical conditions. These findings indicate that the bee gut microbiota has basic roles similar to those found in some other animals and thus provides a model in studies of host–microbe interactions.

https://www.pnas.org/content/pnas/114/18/4775.full.pdf

Honeybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling

The role of the gut microbiome in animal health has become increasingly evident. Unlike most other insects, honey bees possess a highly conserved and specialized core gut microbiome, which consists of nine bacterial species and is acquired mostly through social transmission. Five of these species are ubiquitous in honey bees and are also present in bumble bees. Recent studies have shown that the bee gut microbiome plays a role in metabolism, immune function, growth and development, and protection against pathogens. Disruption of the gut microbiome has also been shown to have detrimental effects on bee health. Overall, evidence suggests that the gut microbiome plays an important role in bee health and disease.

The role of the gut microbiome in health and disease of adult honey bee workers.

It is presently unclear how much individual community members contribute to the overall metabolic output of a gut microbiota. To address this question, we used the honey bee, which harbors a relatively simple and remarkably conserved gut microbiota with striking parallels to the mammalian system and importance for bee health. Using untargeted metabolomics, we profiled metabolic changes in gnotobiotic bees that were colonized with the complete microbiota reconstituted from cultured strains. We then determined the contribution of individual community members in mono-colonized bees and recapitulated our findings using in vitro cultures. Our results show that the honey bee gut microbiota utilizes a wide range of pollen-derived substrates, including flavonoids and outer pollen wall components, suggesting a key role for degradation of recalcitrant secondary plant metabolites and pollen digestion. In turn, multiple species were responsible for the accumulation of organic acids and aromatic compound degradation intermediates. Moreover, a specific gut symbiont, Bifidobacterium asteroides, stimulated the production of host hormones known to impact bee development. While we found evidence for cross-feeding interactions, approximately 80% of the identified metabolic changes were also observed in mono-colonized bees, with Lactobacilli being responsible for the largest share of the metabolic output. These results show that, despite prolonged evolutionary associations, honey bee gut bacteria can independently establish and metabolize a wide range of compounds in the gut. Our study reveals diverse bacterial functions that are likely to contribute to bee health and provide fundamental insights into how metabolic activities are partitioned within gut communities.

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Disentangling metabolic functions of bacteria in the honey bee gut.

The structure and distribution of genomic diversity in natural microbial communities is largely unexplored. Here, we used shotgun metagenomics to assess the diversity of the honey bee gut microbiota, a community consisting of few bacterial phylotypes. Our results show that most phylotypes are composed of sequence-discrete populations, which co-exist in individual bees and show age-specific abundance profiles. In contrast, strains present within these sequence-discrete populations were found to segregate into individual bees. Consequently, despite a conserved phylotype composition, each honey bee harbors a distinct community at the functional level. While ecological differentiation seems to facilitate coexistence at higher taxonomic levels, our findings suggest that, at the level of strains, priority effects during community assembly result in individualized profiles, despite the social lifestyle of the host. Our study underscores the need to move beyond phylotype-level characterizations to understand the function of this community, and illustrates its potential for strain-level analysis.

https://serval.unil.ch/resource/serval:BIB_DD4F991C3500.P001/REF.pdf

Genomic diversity landscape of the honey bee gut microbiota.

It is often taken for granted that all animals host and depend upon a microbiome, yet this has only been shown for a small proportion of species. We propose that animals span a continuum of reliance on microbial symbionts. At one end are the famously symbiont-dependent species such as aphids, humans, corals and cows, in which microbes are abundant and important to host fitness. In the middle are species that may tolerate some microbial colonization but are only minimally or facultatively dependent. At the other end are species that lack beneficial symbionts altogether. While their existence may seem improbable, animals are capable of limiting microbial growth in and on their bodies, and a microbially independent lifestyle may be favored by selection under some circumstances. There is already evidence for several 'microbiome-free' lineages that represent distantly related branches in the animal phylogeny. We discuss why these animals have received such little attention, highlighting the potential for contaminants, transients, and parasites to masquerade as beneficial symbionts. We also suggest ways to explore microbiomes that address the limitations of DNA sequencing. We call for further research on microbiome-free taxa to provide a more complete understanding of the ecology and evolution of macrobe-microbe interactions.

Not all animals need a microbiome.

The highly social (eusocial) corbiculate bees, comprising the honey bees, bumble bees, and stingless bees, are ubiquitous insect pollinators that fulfill critical roles in ecosystem services and human agriculture. Here, we conduct wide sampling across the phylogeny of these corbiculate bees and reveal a dynamic evolutionary history behind their microbiota, marked by multiple gains and losses of gut associates, the presence of generalist as well as host-specific strains, and patterns of diversification driven, in part, by host ecology (for example, colony size). Across four continents, we found that different host species have distinct gut communities, largely independent of geography or sympatry. Nonetheless, their microbiota has a shared heritage: The emergence of the eusocial corbiculate bees from solitary ancestors appears to coincide with the acquisition of five core gut bacterial lineages, supporting the hypothesis that host sociality facilitates the development and maintenance of specialized microbiomes.

https://advances.sciencemag.org/content/advances/3/3/e1600513.full.pdf

Eunice Jia Yu Soh

Papers

Dynamic microbiome evolution in social bees