Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis

Yale University
Gut Microbes 10/2012; 4(1). DOI: 10.4161/gmic.22517
Source: PubMed


The honey bee, Apis mellifera, harbors a characteristic gut microbiota composed of only a few species which seem to be specific to social bees. The maintenance of this stable and distinct microbial community depends on the social lifestyle of these insects. As in other animals, the bacteria in the gut of honey bees probably govern important functions critical to host health. We recently sequenced a metagenome of the gut microbiota of A. mellifera, assigned gene contents to bins corresponding to the major species present in the honey bee gut, and compared functional gene categories between these species, and between the complete metagenome and those of other animals. Gene contents could be linked to different symbiotic functions with the host. Further, we found a high degree of genetic diversity within each of these species. In the case of the gammaproteobacterial species Gilliamella apicola, we could experimentally show a link between genetic variation of isolates and functional differences suggesting that niche partitioning within this species has emerged during evolution with its bee hosts. The consistent presence of only a few species, combined with strain variation within each of these species, makes the gut microbiota of social bees an ideal model for studying functional, structural, and evolutionary aspects of host-associated microbial communities: many characteristics resemble the gut microbiota of humans and other mammals, but the complexity is considerably reduced. In this addendum, we summarize and discuss our major findings and provide a detailed perspective on future research.

20 Reads
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Social honey bees, Apis mellifera, host a set of distinct microbiota, which is similar across the continents and various honey bee species. Some of these bacteria, such as lactobacilli, have been linked to immunity and defence against pathogens. Pathogen defence is crucial, particularly in larval stages, as many pathogens affect the brood. However, information on larval microbiota is conflicting. Seven developmental stages and drones were sampled from 3 colonies at each of the 4 geographic locations of A. mellifera carnica, and the samples were maintained separately for analysis. We analysed the variation and abundance of important bacterial groups and taxa in the collected bees. Major bacterial groups were evaluated over the entire life of honey bee individuals, where digestive tracts of same aged bees were sampled in the course of time. The results showed that the microbial tract of 6-day-old 5th instar larvae were nearly equally rich in total microbial counts per total digestive tract weight as foraging bees, showing a high percentage of various lactobacilli (Firmicutes) and Gilliamella apicola (Gammaproteobacteria 1). However, during pupation, microbial counts were significantly reduced but recovered quickly by 6 days post-emergence. Between emergence and day 6, imago reached the highest counts of Firmicutes and Gammaproteobacteria, which then gradually declined with bee age. Redundancy analysis conducted using denaturing gradient gel electrophoresis identified bacterial species that were characteristic of each developmental stage. The results suggest that 3-day 4th instar larvae contain low microbial counts that increase 2-fold by day 6 and then decrease during pupation. Microbial succession of the imago begins soon after emergence. We found that bacterial counts do not show only yearly cycles within a colony, but vary on the individual level. Sampling and pooling adult bees or 6th day larvae may lead to high errors and variability, as both of these stages may be undergoing dynamic succession.
    PLoS ONE 03/2015; 10(3):e0118707. DOI:10.1371/journal.pone.0118707 · 3.23 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The gut of the Western honey bee, Apis mellifera, is colonized by a characteristic set of bacteria. Two distinct Gammaproteobacteria are consistent members of this unique microbial community, and one has recently been described as a nov. gen., nov. sp. with the name Gilliamella apicola. Here, we present isolation and characterization of PEB0191(T), a strain belonging to the second gammaproteobacterial species present in the honey bee gut microbiota, formerly referred to as Gammaproteobacterium-2. Cells of strain PEB0191(T) are mesophilic with an average length of around 2 μm, and optimal growth was achieved under anaerobic conditions. Growth was not obtained under aerobic conditions and was reduced in a microaerophilic environment. Based on sequence analysis, strain PEB0191(T) belongs to the Orbaceae, and its closest relatives with around 95% sequence similarity are species of the genus Orbus and the genus Gilliamella. Phylogenetic analyses suggest, however, that PEB0191(T) is more closely related to the genus Orbus than to the genus Gilliamella. In accordance with its evolutionary relationship, further similarities between strain PEB0191(T) and other members of the Orbaceae were revealed based on the respiratory quinone type (ubiquinone-8), the fatty acid profile, and the DNA G+C content. Interestingly, like strains of the genus Gilliamella, PEB0191(T) exhibited a high level of resistance against oxytetracycline. The similar levels of sequence divergence from the genera Gilliamella and Orbus and its uncertain phylogenetic position within the family Orbaceae indicate that strain PEB0191(T) represents a novel species of a novel genus with the proposed name Frischella perrara gen. nov., sp. nov.. The type strain is PEB0191(T) (=NCIMB 14821(T)=ATCC BAA-2450(T)).
    International Journal of Systematic and Evolutionary Microbiology 04/2013; 63(Pt 10). DOI:10.1099/ijs.0.049569-0 · 2.51 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: : The gastrointestinal tract in both mammals and insects is associated with microbes (collectively the microbiota), which are controlled by the intestinal immune system. These microbes regulate pathogens that can infect gut epithelial cells, and there is increasing evidence for a reciprocal relationship between beneficial and pathogenic bacteria in the gut and the intestinal immune system. Deciphering these complex interactions between the microbiota and intestinal immune system in mammals requires surrogate model systems, such as larvae of the greater wax moth Galleria mellonella. The exposure of G. mellonella microbiota to antibiotics induces immunity and stress-related genes in the intestine. The model can also provide insight into the virulence mechanisms of pathogens such as Listeria monocytogenes in the human gut and brain. We also discuss the current uses of G. mellonella as a model to develop therapeutic strategies against listeriosis.
    Advances in Biochemical Engineering/Biotechnology 05/2013; DOI:10.1007/10_2013_203 · 1.66 Impact Factor
Show more