The interaction of Serratia bacteria and harmonine in harlequin ladybird confers an interspecies competitive edge
Edited by Nancy Moran, The University of Texas, Austin, TX; received September 13, 2024; accepted November 8, 2024
Significance
Once prized for its use in biological pest control, the harlequin ladybird (Harmonia axyridis) has become an invasive pest in nonnative regions, outcompeting local ladybird species. Here, we found that the harlequin ladybird safely harbors Serratia harmoniae, a highly pathogenic bacterium that causes severe mortality in other ladybird species. The harlequin ladybird’s tolerance to the pathogen is attributed to the defense alkaloid harmonine. Silencing three key genes in the harmonine biosynthesis pathway—Spidey, Sca2, and Desat—reduced the production of harmonine, leading to increased bacterial levels and increased mortality. Penicillin treatment reversed this effect, reducing S. harmoniae content and increasing host survival. This symbiotic host–pathogen relationship confers an intraguild predation advantage to the harlequin ladybird.
Abstract
The harlequin ladybird, Harmonia axyridis, is a predatory beetle used globally to control pests such as aphids and scale insects. Originating from East Asia, this species has become highly invasive since its introduction in the late 19th century to Europe and North America, posing a threat to local biodiversity. Intraguild predation is hypothesized to drive the success of this invasive species, but the underlying mechanisms remain unknown. In this study, a feeding assay revealed that while harlequin ladybirds survive feeding on seven-spotted ladybird eggs, the reverse is not true. However, seven-spotted ladybirds that had fed on harlequin ladybird eggs were able to survive the feeding assay when treated with penicillin. Microbiome sequencing and whole genome analysis of harlequin ladybird eggs revealed a newly discovered pathogenic bacterium strain named Serratia harmoniae. The median lethal concentration (LC50) of S. harmoniae was found to be 2.1 × 105 times higher in the harlequin ladybird compared to the seven-spotted ladybird. The high tolerance observed in harlequin ladybirds was attributed to harmonine, specifically produced in the fat body of this species. Silencing three key genes in the harmonine biosynthesis pathway—Spidey, Sca2, and Desat—reduced the production of the compound, leading to increased S. harmoniae levels and higher mortality. Treating RNAi-altered individuals with penicillin reversed this effect, successfully reducing S. harmoniae presence and increasing insect survival. Taken together, these findings demonstrate that S. harmoniae, a newly identified pathogenic bacterium carried by harlequin ladybirds, interacts with harmonine to confer an interspecies competitive advantage over native ladybird species in nonnative regions.
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Data, Materials, and Software Availability
All raw RNA-seq, 16S sequencing, and genomic datasets generated in this study have been deposited in the NCBI (PRJNA1011000) (89). All other data are included in the manuscript and supporting information.
Acknowledgments
This project was supported by the National Key R&D Program of China (grant numbers 2021YFD1400100 and 2021YFD1400101), the National Natural Science Foundation of China (grant number 32102271), and the China Postdoctoral Science Foundation (grant number 2022T150579). We thank Li Sun from the Fujian Academy of Agricultural Sciences for kindly providing Harmonia dimidiata samples. We thank Xue-xin Chen of Zhejiang University and Nian-wan Yang of the Chinese Academy of Agricultural Sciences for their advice.
Author contributions
C.Z., H.Z., K.H., and F.L. designed research; C.Z., H.Z., Y.X., M.C., Y.G., and S.J. performed research; Y.M. contributed new reagents/analytic tools; C.Z., H.Z., Z.Z., and R.S. analyzed data; and C.Z., H.Z., B.H., and F.L. wrote the paper.
Competing interests
The authors declare no competing interest.
Supporting Information
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Copyright © 2024 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
Data, Materials, and Software Availability
All raw RNA-seq, 16S sequencing, and genomic datasets generated in this study have been deposited in the NCBI (PRJNA1011000) (89). All other data are included in the manuscript and supporting information.
Submission history
Received: September 13, 2024
Accepted: November 8, 2024
Published online: December 30, 2024
Published in issue: January 14, 2025
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Acknowledgments
This project was supported by the National Key R&D Program of China (grant numbers 2021YFD1400100 and 2021YFD1400101), the National Natural Science Foundation of China (grant number 32102271), and the China Postdoctoral Science Foundation (grant number 2022T150579). We thank Li Sun from the Fujian Academy of Agricultural Sciences for kindly providing Harmonia dimidiata samples. We thank Xue-xin Chen of Zhejiang University and Nian-wan Yang of the Chinese Academy of Agricultural Sciences for their advice.
Author contributions
C.Z., H.Z., K.H., and F.L. designed research; C.Z., H.Z., Y.X., M.C., Y.G., and S.J. performed research; Y.M. contributed new reagents/analytic tools; C.Z., H.Z., Z.Z., and R.S. analyzed data; and C.Z., H.Z., B.H., and F.L. wrote the paper.
Competing interests
The authors declare no competing interest.
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The interaction of Serratia bacteria and harmonine in harlequin ladybird confers an interspecies competitive edge, Proc. Natl. Acad. Sci. U.S.A.
122 (2) e2417873121,
https://doi.org/10.1073/pnas.2417873121
(2025).
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