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.

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    • "For example, the microbiome in the human gut has been linked with a healthy function of the brain, the immune system, the digestive system, and with a number of diseases ranging from cancer to metabolic or even psychiatric disorders (Foster & McVey Neufeld, 2013; Biedermann & Rogler, 2015; Dash et al., 2015; Viaud et al., 2015). In animals, the microbiome has been associated with similar functions in development and disease (Engel & Moran, 2013; Kostic et al., 2013; Sabree & Moran, 2014). A lot of interest has also been given to microbes associated with surfaces of roots or leaves (Andrews & Harris, 2000; Lindow & Brandl, 2003; Vorholt, 2012; Humphrey et al., 2014). "
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    ABSTRACT: We have explored the importance of the phyllosphere microbiome in plant resistance in the cuticle mutants bdg (BODYGUARD) or lacs2.3 (LONG CHAIN FATTY ACID SYNTHASE 2) that are strongly resistant to the fungal pathogen Botrytis cinerea. The study includes infection of plants under sterile conditions, 16S ribosomal DNA sequencing of the phyllosphere microbiome, and isolation and high coverage sequencing of bacteria from the phyllosphere. When inoculated under sterile conditions bdg became as susceptible as wild-type (WT) plants whereas lacs2.3 mutants retained the resistance. Adding washes of its phyllosphere microbiome could restore the resistance of bdg mutants, whereas the resistance of lacs2.3 results from endogenous mechanisms. The phyllosphere microbiome showed distinct populations in WT plants compared to cuticle mutants. One species identified as Pseudomonas sp isolated from the microbiome of bdg provided resistance to B. cinerea on Arabidopsis thaliana as well as on apple fruits. No direct activity was observed against B. cinerea and the action of the bacterium required the plant. Thus, microbes present on the plant surface contribute to the resistance to B. cinerea. These results open new perspectives on the function of the leaf microbiome in the protection of plants.
    Full-text · Article · Jan 2016 · New Phytologist
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    • "Similarly, pectinase, an enzyme that breaks down pectin (a heteropolysaccharide found in plant cell walls), has biotechnological potential in extracting fruit juice (e.g., apple juice) and in wine production. Honey bees host symbiotic Gamma- Proteobacteria that possess the genetic potential for pectin degradation and show in vitro production of pectinase to break down pollen cell walls (Engel and Moran 2012). In leafcutting ants, pectinolytic enzymes that are ingested from the fungal cultivar pass unaffected through the ant gut and are finally applied to the plant substrates used for fungal cultivation (Schiøtt et al. 2010). "
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    ABSTRACT: Symbiotic interactions between insects and microorganisms are widespread in nature and are often the source of ecological innovations. In addition to supplementing their host with essential nutrients, microbial symbionts can produce enzymes that help degrade their food source as well as small molecules that defend against pathogens, parasites, and predators. As such, the study of insect ecology and symbiosis represents an important source of chemical compounds and enzymes with potential biotechnological value. In addition, the knowledge on insect symbiosis can provide novel avenues for the control of agricultural pest insects and vectors of human diseases, through targeted manipulation of the symbionts or the host-symbiont associations. Here, we discuss different insect-microbe interactions that can be exploited for insect pest and human disease control, as well as in human medicine and industrial processes. Our aim is to raise awareness that insect symbionts can be interesting sources of biotechnological applications and that knowledge on insect ecology can guide targeted efforts to discover microorganisms of applied value.
    Full-text · Article · Dec 2015 · Applied Microbiology and Biotechnology
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    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.
    Full-text · Article · Mar 2015 · PLoS ONE
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