Abstract
Symbiont-mediated nutritional mutualisms can contribute to the host fitness of insects, especially for those that feed exclusively on nutritionally unbalanced diets. Here, we elucidate the importance of B group vitamins in the association of endosymbiotic bacteria Wolbachia with two plant-sap feeding insects, the small brown planthopper, Laodelphax striatellus (Fallén), and the brown planthopper, Nilaparvata lugens (Stål). Infected planthoppers of both species laid more eggs than uninfected planthoppers, while the experimental transfer of Wolbachia into uninfected lines of one planthopper species rescued this fecundity deficit. The genomic analysis showed that Wolbachia strains from the two planthopper species encoded complete biosynthesis operons for biotin and riboflavin, while a metabolic analysis revealed that Wolbachia-infected planthoppers of both species had higher titers of biotin and riboflavin. Furthermore, experimental supplementation of food with a mixture of biotin and riboflavin recovered the fecundity deficit of Wolbachia-uninfected planthoppers. In addition, comparative genomic analysis suggested that the riboflavin synthesis genes are conserved among Wolbachia supergroups. Biotin operons are rare in Wolbachia, and those described share a recent ancestor that may have been horizontally transferred from Cardinium bacteria. Our research demonstrates a type of mutualism that involves a facultative interaction between Wolbachia and plant-sap feeding insects involving vitamin Bs.
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Data availability
The draft genome sequences data are freely available in NCBI GenBank under accession numbers MUIY00000000 (wLug) and MUIX00000000 (wStriCN).
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Acknowledgements
We thank Professor John Werren of the University of Rochester, USA for his comments on the paper, and Dr Jing-Tao Sun, Tong-Pu Li, and Pei-Wen Mo of Nanjing Agricultural University, China for their help on this project. This work was supported by the National Natural Science Foundation of China (Nos. 31672035 and 31871976) to X-YH and the startup grant from Nanjing Agricultural University to X-LB (No. 804015).
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JFJ, XLB, and XYH designed the research; JFJ, XLB, YG, DSZ, KJZ, HJH, JTG, XZ, ZX, AH, and XYH performed the research; JFJ, XLB, DSZ, JJH, ZX, AH, and XYH wrote and edited the paper. All authors read and approved the paper.
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Ju, JF., Bing, XL., Zhao, DS. et al. Wolbachia supplement biotin and riboflavin to enhance reproduction in planthoppers. ISME J 14, 676–687 (2020). https://doi.org/10.1038/s41396-019-0559-9
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DOI: https://doi.org/10.1038/s41396-019-0559-9
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