Disentangling metabolic functions of bacteria in the honey bee gut

Abstract

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.

The gut microbiome is associated with behavioural task in honey bees

“…Moreover, both groups of bacteria have recently been shown to utilize secondary plant metabolites from the outer pollen wall, such as flavonoids, phenolamides, and ω-hydroxy acids (Kešnerová et al 2017). Potentially these bacterial taxa may be more strongly selected for in in nest workers that consume a more pollen-rich diet (Crailsheim et al 1992), and that perform tasks within the hive such as feeding the brood.…”

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity

“…gut communities (Kwong, Engel, Koch, & Moran, 2014). In the gut of the European honey bee (A. mellifera), S. alvi is thought to utilize carboxylic acids as an energy source (Kešnerová et al, 2017), but any positive or negative effects of this bacterium on its host have so far not been described.…”

“…Experiments manipulating the microbiome could establish whether there is a causal link between community diversity and colony productivity in T. nylanderi. Studies that have radically disrupted bacterial communities in both social and nonsocial insects by administering antibiotics have found strong fitness effects (e.g., Jaffé et al, 2001;Nogge & Gerresheim, 1982;Rosengaus, Zecher, Schultheis, Brucker, & Bordenstein, 2011), though ideally controlled inoculations with bacterial strains should be performed to test for the effects of the community composition on the host (e.g., Kešnerová et al, 2017;Schwab et al, 2016).…”

An interaction between host and microbe genotypes determines colonization success of a key bumble bee gut microbiota member

“…Recent advances have shed light on the important contributions of microbial communities for the health and evolutionary fitness of their hosts. These microbiota have implications for host defense (Dong et al 2009;Oliver et al 2012;Parker et al 2017), development (Visick et al 2000;Palm et al 2015), and physiology (Kikuchi et al 2012;Brune 2014;Kešnerová et al 2017). The role of an organism's microbiota in determining fitness-relevant host traits necessitates an understanding of ecological and evolutionary determinants of the composition of these microbial communities, including a focus on factors that drive the colonization and establishment of particular microbes.…”