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Engineering bacterial symbionts of nematodes improves their biocontrol potential to counter the western corn rootworm

Nature Biotechnology volume 38, pages 600–608 (2020)Cite this article

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A Publisher Correction to this article was published on 12 March 2020

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Abstract

The western corn rootworm (WCR) decimates maize crops worldwide. One potential way to control this pest is treatment with entomopathogenic nematodes (EPNs) that harbor bacterial symbionts that are pathogenic to insects. However, WCR larvae sequester benzoxazinoid secondary metabolites that are produced by maize and use them to increase their resistance to the nematodes and their symbionts. Here we report that experimental evolution and selection for bacterial symbionts that are resistant to benzoxazinoids improve the ability of a nematode–symbiont pair to kill WCR larvae. We isolated five Photorhabdus symbionts from different nematodes and increased their benzoxazinoid resistance through experimental evolution. Benzoxazinoid resistance evolved through multiple mechanisms, including a mutation in the aquaporin-like channel gene aqpZ. We reintroduced benzoxazinoid-resistant Photorhabdus strains into their original EPN hosts and identified one nematode–symbiont pair that was able to kill benzoxazinoid-sequestering WCR larvae more efficiently. Our results suggest that modification of bacterial symbionts might provide a generalizable strategy to improve biocontrol of agricultural pests.

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Fig. 1: Overview of the study system.
Fig. 2: Selection on MBOA increases MBOA resistance of different Photorhabdus strains.
Fig. 3: Increased MBOA resistance is associated with various mutations.
Fig. 4: Complementation with WT aqpZ gene restores MBOA susceptibility in an MBOA-resistant aqpZ-mutant strain.
Fig. 5: Selection on MBOA alters symbiotic capability of a subset of bacterial strains.
Fig. 6: Nematodes harboring MBOA-resistant symbionts show improved biocontrol of benzoxazinoid-sequestering WCR larvae.

Data availability

Genome sequences were deposited in the National Center for Biotechnology Information (NCBI) databank. They can be retrieved using the following accession numbers: TT01-23: WSFH00000000, C-TT01: WSEZ00000000, M-TT01: WSFG00000000, IL9: WSFB00000000, C-IL9: WSEX00000000, M-IL9: WSFF00000000, M-CN4: WSFC00000000, EN01: WSFA00000000, C-EN01: WSEV00000000, M-EN01: WSFD00000000, CN4: WSEY00000000, C-CN4: WSEU00000000, HU2: NSCN00000000, C-HU2: WSEW00000000, M-HU2: WSFE00000000. Sanger sequence traces can be found at https://doi.org/10.5061/dryad.mgqnk98w4. The nematode strains CN4, IL9, EN01 and HU2 were obtained under a material transfer agreement from e-nema (Germany). TT01 nematodes are available from different laboratories and were provided by D. Clarke (University College Cork). Selected bacteria and nematodes are available upon reasonable request and the successful completion of material transfer agreements with the authors and third parties as suppliers of the source materials. Data are available in the main text and the supplementary materials. All raw datasets were deposited in Dryad: https://doi.org/10.5061/dryad.mgqnk98w4.

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Acknowledgements

We thank the Next Generation Sequencing Platform and the Interfaculty Bioinformatics Unit of the University of Bern for performing whole-genome sequencing and providing the high-performance computing infrastructure. We also thank M. Fragniere and S. Schenk for their help with sequencing; D. Ermacora and A. Boss for technical assistance; R.-U. Ehlers (e-nema, Germany) and D. Clarke (University College Cork, Ireland) for contributing nematode and bacterial strains; C. Easom, D. Clarke, C. Hertz and L. Hu for contributing photographs; and the members of the Research Section Biotic Interactions of the Institute of Plant Sciences of the University of Bern for their support and helpful discussions. This project was supported by the Swiss National Science Foundation (grants 155781, 160786, 157884 and 169791) and the University of Bern through the Interfaculty Research Cooperation One Health. Work in the Bode lab was supported by the LOEWE Center TBG, funded by the state of Hesse.

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Authors and Affiliations

  1. Institute of Plant Sciences, University of Bern, Bern, Switzerland

    Ricardo A. R. Machado, Lisa Thönen, Carla C. M. Arce, Vanitha Theepan, Fausto Prada, Christelle A. M. Robert, Evangelia Vogiatzaki & Matthias Erb

  2. Institute of Biology, University of Neuchâtel, Neuchâtel, Switzerland

    Carla C. M. Arce

  3. Interfaculty Bioinformatics Unit, University of Bern, Bern, Switzerland

    Daniel Wüthrich & Rémy Bruggmann

  4. Molekulare Biotechnologie, Fachbereich Biowissenschaften, Goethe-Universität Frankfurt am Main, Frankfurt, Germany

    Yi-Ming Shi & Helge B. Bode

  5. Buchmann Institute for Molecular Life Sciences (BMLS), Goethe-Universität Frankfurt, Frankfurt, Germany

    Yi-Ming Shi & Helge B. Bode

  6. LOEWE Translational Biodiversity Genomics (TBG), Frankfurt, Germany

    Yi-Ming Shi & Helge B. Bode

  7. Institute for Infectious Diseases, University of Bern, Bern, Switzerland

    Olivier P. Schaeren, Matheus Notter & Siegfried Hapfelmeier

  8. Graduate School GCB, University of Bern, Bern, Switzerland

    Olivier P. Schaeren & Matheus Notter

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Contributions

R.A.R.M. conceived the original project, designed, supervised and performed experiments, analyzed data and wrote the first draft of the manuscript. L.T. performed experiments and analyzed data. C.C.M.A. designed, supervised and performed experiments and analyzed data. V.T. and F.P. performed experiments. D.W. analyzed data. C.A.M.R. supervised and performed experiments. E.V., Y.-M.S., O.P.S. and M.N. performed experiments. R.B. analyzed data and provided infrastructure. S.H. and H.B.B. provided protocols, experimental material and infrastructure. M.E. conceived the original project, designed experiments, analyzed data, provided infrastructure and wrote the first draft of the manuscript. All authors contributed to the final version of the manuscript.

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Correspondence to Ricardo A. R. Machado.

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Machado, R.A.R., Thönen, L., Arce, C.C.M. et al. Engineering bacterial symbionts of nematodes improves their biocontrol potential to counter the western corn rootworm. Nat Biotechnol 38, 600–608 (2020). https://doi.org/10.1038/s41587-020-0419-1

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