Dataset Information

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.

SUBMITTER: Kesnerova L

PROVIDER: S-EPMC5726620 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Disentangling metabolic functions of bacteria in the honey bee gut.

Kešnerová Lucie L Mars Ruben A T RAT Ellegaard Kirsten M KM Troilo Michaël M Sauer Uwe U Engel Philipp P

PLoS biology 20171212 12

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 th ...[more]

PMID: 29232373

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Project description:IntroductionThe functional relevance of intra-species diversity in natural microbial communities remains largely unexplored. The guts of two closely related honey bee species, Apis cerana and A. mellifera, are colonised by a similar set of core bacterial species composed of host-specific strains, thereby providing a good model for an intra-species diversity study.ObjectivesWe aim to assess the functional relevance of intra-species diversity of A. cerana and A. mellifera gut microbiota.MethodsHoney bee workers were collected from four regions of China. Their gut microbiomes were investigated by shotgun metagenomic sequencing, and the bacterial compositions were compared at the species level. A cross-species colonisation assay was conducted, with the gut metabolomes being characterised by LC-MS/MS.ResultsComparative analysis showed that the strain composition of the core bacterial species was host-specific. These core bacterial species presented distinctive functional profiles between the hosts. However, the overall functional profiles of the A. cerana and A. mellifera gut microbiomes were similar; this was further supported by the consistency of the honey bees' gut metabolome, as the gut microbiota of different honey bee species showed rather similar metabolic profiles in the cross-species colonisation assay. Moreover, this experiment also demonstrated that the gut microbiota of A. cerana and A. mellifera could cross colonise between the two honey bee species.ConclusionOur findings revealed functional differences in most core gut bacteria between the guts of A. cerana and A. mellifera, which may be associated with their inter-species diversity. However, the functional profiles of the overall gut microbiomes between the two honey bee species converge, probably as a result of the overlapping ecological niches of the two species. Our findings provide critical insights into the evolution and functional roles of the mutualistic microbiota of honey bees and reveal that functional redundancy could stabilise the gene content diversity at the strain-level within the gut community.

Project description:Temperate honey bees (Apis mellifera) are challenged by low temperatures and abrupt dietary shifts associated with behavioral changes during winter. Case studies have revealed drastic turnover in the gut microbiota of winter bees, highlighted by the seasonal dominance of a non-core bacterium Bartonella. However, neither biological consequence nor underlying mechanism of this microbial turnover is clear. In particular, we ask whether such changes in gut profile are related to winter dietary shift and possibly beneficial to host and associated gut microbiome? Here, we integrated evidences from genomics, metagenomics, and metabolomics in three honey bee subspecies maintained at the same locality of northern China to profile both diversity and functional variations in gut bacteria across seasons. Our results showed that winter dominance of Bartonella was shared in all tested honey bee lineages. This seasonal change was likely a consequence of winter dietary shifts characterized by greatly reduced pollen consumption and accumulation of metabolic waste due to restricted excretion. Bartonella showed expanded genomic capacity in utilizing more diverse energy substrates, such as converting metabolic wastes lactate and ethanol into pyruvate, an energy source for self-utilization and possibly also for host and other symbionts. Furthermore, Bartonella was the only bacterium capable of both producing and secreting tryptophan and phenylalanine, whose metabolic products were detected in bee guts, even though all gut bacteria lacked relevant digestion enzymes. These results thus suggested a possible mechanism where the gut bacteria might benefit the host by supplementing them with essential amino acids lacking in a protein shortage diet. IMPORTANCE The abilities to survive winter and to adapt to major food changes are key traits that have enabled successful range expansion of the honey bees from the tropic to temperate climate. Our results highlighted a new possibility that gut bacteria may have played an important role in host survival of the severe winter condition. The non-core bacterium Bartonella is not only more adaptive to the winter diet but is also equipped with the capacity to provide the host with essential nutrients and important metabolic substrates. This overall host-bacterium profile is probably favored by natural selection, resulting in a consistent winter gut strategy across varied honey bee lineages. Conversely, when the hosts start to forage again, core bacteria maintained at low abundance during winter returned to their typical dominant status, thus completing the annual gut turnover. Our study suggests a new hypothesis where seasonal gut variations may improve the fitness of the honey bee, allowing them to explore more diverse climates.

Dataset Information

Disentangling metabolic functions of bacteria in the honey bee gut.

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Disentangling metabolic functions of bacteria in the honey bee gut.

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