Honey bees are exposed to a myriad of environmental stressors, including agrochemicals, plant toxins and variable diet components, which may exert a wide range of effects on their health. Some of these effects may directly compromise bees by decreasing their survival rates, while others may indirectly compromise bee health by perturbing the gut microbiota and/or weakening the immune system. My research group investigates the effects of specific toxins on the bee gut microbiota. These include (1) agrochemicals, such as antibiotics, herbicides, fungicides, and insecticides, and (2) plant toxins, such as alkaloids, cyanogenic glycosides and flavonoid glycosides. These chemicals may impact microbial composition and abundance in the bee gut and may potentially affect host susceptibility to opportunistic pathogens. On the other hand, they may be metabolized by specific members of the gut microbiota, and the byproducts may be beneficial, neutral, or harmful to bees. My research work involves in vitro experiments with bee-associated bacteria to investigate their susceptibility to and ability to metabolize xenobiotics, and in vivo studies in which bees are exposed to field-relevant concentrations of toxins to investigate their short-term and long-term impact on the gut microbiota. Impacts are investigated by metagenomics, transcriptomics, and proteomics analyses. We also investigate the consequences of dysbiosis to host health, by performing infection assays and monitoring changes in gut microbial community and host survivorship after exposure to both chemical and opportunistic pathogen.
Related work:
Motta EVS, Gage A*, de Jong TK*, Edwards JA, Moran NA. (2024) Glyphosate effects on growth and biofilm formation in bee gut symbionts and diverse associated bacteria. Applied and Environmental Microbiology e00515-24 * Mentees
Motta EVS, Arnott RWL, Moran NA. (2023) Caffeine consumption helps honey bees fight a bacterial pathogen. Microbiology Spectrum e00520-23
Motta EVS & Moran NA. (2023) The effects of glyphosate, pure or in herbicide formulation, on bumble bees and their gut microbial communities. Science of the Total Environment 872: 162102
Motta EVS, Powell JE, Moran NA. (2022) Glyphosate induces immune dysregulation in honey bees. Animal Microbiome 4(16): 1-14
Motta EVS, Mak M*, de Jong TK*, Powell JE, O'donnell A, Suhr KJ, Riddington IM, Moran NA. (2020) Oral or topical exposure to glyphosate in herbicide formulation impacts the gut microbiota and survival rates of honey bees. Applied and Environmental Microbiology 86: e01150-20
Motta EVS & Moran NA. (2020) Impact of glyphosate on the honey bee gut microbiota: effects of intensity, duration and timing of exposure. mSystems 5: e00268-20
Motta EVS, Raymann K, Moran NA. (2018) Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences of the United States of America 115(41): 10305-10310
Raymann K#, Motta EVS#, Girard C#, Riddington IM, Dinser JA, Moran NA. (2018) Imidacloprid decreases honey bee survival rates but does not affect the gut microbiome. Applied and Environmental Microbiology 84(13): e00545-18 #Authors contributed equally to the work
Host and microbiota interactions
The ability of bacteria to colonize niches within the gut is influenced by host-defined factors, but also appears to reflect the outcomes of antagonistic interactions among bacterial strains and species. These interactions may be contact-dependent, such as those mediated by type VI secretion systems (T6SSs), or contact-independent, exemplified by the production of bacteriocins. Bacterial symbionts in the bee gut utilize T6SSs to compete with other microorganisms, enhancing their survival in this complex environment. T6SSs are intricate structures found in specific Gram-negative bacteria that facilitate the delivery of toxic effector proteins to neighboring cells, thereby influencing competition and survival outcomes. Additionally, these symbionts can produce and secrete antimicrobial compounds that serve as weapons against pathogens or as mechanisms for establishing their presence within the bee gut. Our research employs a comprehensive approach that integrates genetic engineering, in vitro and in vivo experiments, and multi-omics techniques to elucidate how mutualistic bacteria leverage these capabilities to colonize the gut, interact with one another, and modulate host physiological pathways.
Related work:
Motta EVS, Lariviere PJ, Jones KR, Song Y, Moran NA. (2024) Type VI secretion systems promote intraspecific competition and host interactions in a bee gut symbiont. PNAS 121(44): e2414882121
Motta EVS & Moran NA. (2024) The honey bee microbiota and its impact on health and disease. Nature Reviews Microbiology 22(3): 122-137
Motta EVS, Gage A, Smith TE, Blake KJ, Kwong WK, Riddington IM, Moran NA. (2022) Host-microbiome metabolism of a plant toxin in bees. eLife 11:e82595
Steele M, Motta EVS, Gattu T, Martinez D, Moran NA. (2021) The gut microbiota protects bees from invasion by a bacterial pathogen. Microbiology Spectrum 9: e00394-21
Zheng H, Steele MI, Leonard SP, Motta EVS, Moran NA. (2018) Honey bees as models for gut microbiota research. Lab Animal 47(11): 317-315
The use of probiotics aimed at treating or preventing microbial infections in hives is common in beekeeping. Most commercially available honey bee probiotics consist of non-native microorganisms, including bacteria and fungi from the food industry, which are marketed as promoting bee health. However, there is little evidence suggesting that these microbes colonize the honey bee gut. An alternative approach that has been proposed more recently involves probiotics consisting of native bacterial symbionts that colonize and persist in the honey bee gut. Orally delivered gut homogenates are one way to transfer bacteria from healthy worker bees to bees lacking microbiota or with perturbed microbiota. Gut homogenate treatments lead to stable colonization in young bees under laboratory conditions, but potentially introduce pathogens from donor bees. Defined communities of isolates of native core bacteria are another approach that has been employed by some research groups. My research team will investigate whether these defined communities can counteract perturbations caused by agrochemicals and other environmental stressors and prevent the proliferation of opportunistic pathogens that often follow perturbation. We will conduct both laboratory and hive-level experiments as an attempt to evaluate the efficacy of probiotics for beekeeping.
Related work:
Motta EVS, Powell JE, Leonard SP, Moran NA. (2022) Prospects for probiotics in social bees. Philosophical Transactions of the Royal Society B: Biological Sciences 377(1853): 20210156