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Pollen-inspired enzymatic microparticles to reduce organophosphate toxicity in managed pollinators

Abstract

Pollinators support the production of the leading food crops worldwide. Organophosphates are a heavily used group of insecticides that pollinators can be exposed to, especially during crop pollination. Exposure to lethal or sublethal doses can impair fitness of wild and managed bees, risking pollination quality and food security. Here we report a low-cost, scalable in vivo detoxification strategy for organophosphate insecticides involving encapsulation of phosphotriesterase (OPT) in pollen-inspired microparticles (PIMs). We developed uniform and consumable PIMs capable of loading OPT at 90% efficiency and protecting OPT from degradation in the pH of a bee gut. Microcolonies of Bombus impatiens fed malathion-contaminated pollen patties demonstrated 100% survival when fed OPT−PIMs but 0% survival with OPT alone, or with plain sucrose within five and four days, respectively. Thus, the detrimental effects of malathion were eliminated when bees consumed OPT−PIMs. This design presents a versatile treatment that can be integrated into supplemental feeds such as pollen patties or dietary syrup for managed pollinators to reduce risk of organophosphate insecticides.

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Fig. 1: A schematic of the passage of microparticles through a bee digestive tract.
Fig. 2: Characterizations of the stability, size distribution and morphology of PIMs.
Fig. 3: Characterizations of OPT encapsulation and activity in PIMs.
Fig. 4: Tracking of digested PIMs by fluorescent imaging of bumblebee GI tracts.
Fig. 5: Characterization of OPT−PIM efficacy through AChE activity assay and bee survival experiments.

Data availability

The data that support the findings of this study are available from the corresponding author on request. Source data are provided with this paper.

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Acknowledgements

This material is based on work that are partially supported by the National Institute of Food and Agriculture, US Department of Agriculture, Hatch under 2017-18-107, Counter ACT Program of the National Institute of Health under Award Number R21-NS10383-01 and the National Science Foundation under Award Number IIP-1918981. This work made use of the Cornell Center for Materials Research Shared Facilities which are supported through the NSF MRSEC programme (DMR-1719875).

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Contributions

J.C. and M.M. conceived the study. J.C. and J.W. designed and conducted the experiments. S.G. and J.-K.M. provided the E. coli strain. K.S. drew the schemes. J.C., J.W., J.-K.M., S.M. and M.M. reviewed and interpreted the results. J.C, J.W. and M.M. wrote the manuscript, with input from all authors. All authors reviewed and commented on the manuscript.

Corresponding author

Correspondence to Minglin Ma.

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Competing interests

The technology described in this paper is being licensed to Beemmunity Inc., a start-up company co-founded by J.W. M.M. and J.C. are scientific advisors and shareholders of Beemmunity Inc.

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Peer review information Nature Food thanks Liangfang Zhang, Scott Walper and Scott Medina for their contribution to the peer review of this work.

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Source data

Source Data Fig. 2

Size distribution, suspension stability and pore size distribution.

Source Data Fig. 3

Protein loading efficiency and relative enzyme activity.

Source Data Fig. 5

Relative activity of AChE and survival data.

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Chen, J., Webb, J., Shariati, K. et al. Pollen-inspired enzymatic microparticles to reduce organophosphate toxicity in managed pollinators. Nat Food 2, 339–347 (2021). https://doi.org/10.1038/s43016-021-00282-0

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