Less but not least?

Compartmentalization of the honeybee gut microbiota occurs not only for the main bacterial members, but also for fungi and less abundant environmental bacteria. This specific pattern of distribution indicates that they are not simply acquired by the diet but they are adapted to gut compartments.

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Honeybees (Apis mellifera) are the main and most economically relevant group of pollinators, whose presence in agroecosystems considerably boosts crop productivity, and keep our tables set with fruits and vegetables. Together with other pollinators, including wild bees, they also provide wild plants with the important ecological service of pollination, and they play a crucial role for the maintenance of plant species diversity (1).

 As many other insects, honeybees have established strict associations with microorganisms, which contribute to the overall functionality and well-being of the host (2). Compared to mammalian gut associated microorganisms, the ones in honeybee gut represent a simpler community to investigate; therefore, they are considered as a model system to study the microbial interactions with host, but also a model to explore the interplay among the microbial partners. Advances in analytical molecular technologies, as well as the application of multiple techniques, such as microbial cultivation, recolonization experiments of the insect with selected strains, and metabolomics, allowed a better insight into the honeybee microbial community. Even if with an extensive strain-level variation, it has been showed that the high proportion (about 95%–99%) of A. mellifera gut microbiota is made up by nine bacterial dominant types. Previous studies showed that these dominant types are constant across different adult bee populations (2, 3). All these species can be grown in laboratory conditions, and they show a specific distribution along gut compartments (different physical portions of gut; i.e., crop, midgut, rectum, and ileum). In addition, they have an important role for the honey bee metabolism, because they take part to digestive process, modulate the insect immune response, and detoxicate from harmful compounds (2). So far, researchers have devoted many efforts to the study of these dominant bacterial partners (2). But, what about the fungal members and the non-core, less abundant environmental bacteria? Do they have the same compartment-specific distribution shown by the dominant ones or are they randomly scattered throughout the entire gut? Our study originated from these questions, and from the consideration that, as different works reported,members of the so-called “rare microbial biosphere” (i.e., the less abundant microbial species present in an environment or niche) may be crucial in natural ecosystems and for the host health (4). In this study we elucidated the structure of the honeybee gut microbiota, focusing on the bacterial and fungal components. We observed a specific pattern of localization, not only for the dominant bacteria, but also for the less prevalent environmental bacteria and fungi, along with a variation of the physico-chemical conditions existing in the different gut sections (Figure below).Based on these results, we hypothesized that these minor components represent a reservoir of functions that can integrate the abilities of the abundant one sustain bee health. This detailed and refined description of the microbiota structure and “compartmentalization” can indeed put the less prevalent microbial partners in a different light, unlocking solutions to improve honeybee health against stressors.

Considering the importance of these insects at different levels, bee colonies loss caused by a wide variety of biotic and abiotic factors, and by their interactions (e.g., global warming, exposure to agriculture chemicals and disease outbreaks) represents a significant problem with both economic and environmental fall-outs. Recent research has underlined that the maintenance of a healthy gut microbiota is essential to help bees to counteract stressors, such as pathogens (5) or pesticides that can disrupt the natural bee microbiota (6). In this contest, our results can provide the basis for future investigations about the ways fungi and environmental bacteria interact with the host or how these non-core and less abundant microbiome components contribute to gut homeostasis. Examples of non-core environmental bacteria that can indeed provide benefits are known: bacterial strains isolated from honeybee gut belonging to the family Lactobacillaceae were found to protect the host from pathogens such as Paenibacillus larvae (7). This work also emphasizes the importance of considering the ecological landscape where the bees live, and from which they acquire the less prevalent microbial partners. An ecological diverse and integrated landscape protects and promotes the diversity of plant species and habitats. Consequently, this landscape may improve the diversity of microorganisms that honeybees may encounter, and that eventually can interact with the more abundant ones.

References

  1. Gallai et al., Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68, 810821 (2009).
  2. K. Kwong, N. A. Moran, Gut microbial communities of social bees. Nature Reviews Microbiology 14, 374–384 (2016).
  3. K. Kwong et al., Dynamic microbiome evolution in social bees. Science Advances 3, e1600513 (2017).
  4. Jousset et al., Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J 11, 853–862 (2017).
  5. Raymann and N. A. Moran, The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science 26, 97–104 (2018).
  6. V. S. Motta, K. Raymann, N. A. Moran. Glyphosate perturbs the gut microbiota of honey bees. PNAS 115, 10305–10310 (2018).
  7. Forgren et al., Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41, 99–108 (2010).

Ramona Marasco

Researcher, KAUST