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The interaction of Serratia bacteria and harmonine in harlequin ladybird confers an interspecies competitive edge
Thursday, 2025/01/23 | 07:49:20
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Chaowei Zhang, Hang Zhou, Kang He, Yiqi Xiao, Mengyao Chen, Zhangqi Zuo, Runguo Shu, PNAS December 30, 2024; 122 (2) e2417873121; https://doi.org/10.1073/pnas.2417873121 SignificanceOnce 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. AbstractThe 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.
See https://www.pnas.org/doi/10.1073/pnas.2417873121
Figure 4: Mechanisms of harmonine protection against S. harmoniae. The C16 precursor is obtained through the hydrolysis of lipid droplets and subsequently enters the endoplasmic reticulum in the presence of Malonyl-CoA, contributing to fatty acid elongation and the formation of stearic acid. This is catalyzed by a HaDesat-mediated enzyme to form oleic acid, which undergoes a series of oxidative, dehydrating, and amination reactions, resulting in harmonine production. Harmonine is then released to extracellular spaces along with body fluids to resist S. harmoniae.
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