Abstract
Insect symbionts are widespread in nature and lateral gene transfer is prevalent in insect symbiosis. However, the function of horizontally transferred genes (HTGs) in insect symbiosis remains speculative, including the mechanism that enables insects to feed on plant phloem deficient in B vitamins. Previously, we found there is redundancy in biotin synthesis pathways from both whitefly Bemisia tabaci and symbiotic Hamiltonella due to the presence of whitefly HTGs. Here, we demonstrate that elimination of Hamiltonella decreased biotin levels but elevated the expression of horizontally transferred biotin genes in whiteflies. HTGs proteins exhibit specific expression patterns in specialized insect cells called bacteriocytes housing symbionts. Complementation with whitefly HTGs rescued E. coli biotin gene knockout mutants. Furthermore, silencing whitefly HTGs in Hamiltonella-infected whiteflies reduced biotin levels and hindered adult survival and fecundity, which was partially rescued by biotin supplementation. Each of horizontally transferred biotin genes are conserved in various laboratory cultures and species of whiteflies with geographically diverse distributions, which shares an evolutionary origin. We provide the first experimental evidence that biotin synthesized through acquired HTGs is important in whiteflies and may be as well in other animals. Our findings suggest that B vitamin provisioning in animal-microbe symbiosis frequently evolved from bacterial symbionts to animal hosts through horizontal gene transfer events. This study will also shed light on how the animal genomes evolve through functional transfer of genes with bacterial origin in the wider contexts of microbial ecology.
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Acknowledgements
We would like to thank Professor Myron Zalucki of the University of Queensland, Australia for his constructive comments and suggestions on the paper. The authors thank Professor Liu Shu-Sheng for providing the whitefly B. tabaci MEAM1 culture, and Dr. Lu Gang, Bao Xi-Yu, Li Ce, Li Chu-Qiao, and Wang Yan-Bin for their assistance with the experiments. This work was supported by the National Natural Science Foundation of China (No. 31871967), High-Tech R&D Program of Liaoning (No. 2019JH2/10200012), and High-Level Talent Support Foundation from Liaoning, Shenyang and Shenyang Agricultural University (Project XLYC1902104, RC180025 and 880418001).
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JBL conceived the study. FRR conducted symbiont elimination, biotin assays, ecology experiments, gene expression analyses, and gene silencing. FRR, XS, TYW, and XZ performed the complementation experiments. XS carried out gene silencing, FISH and immunofluorescence experiments. YLY constructed the phylogenetic tree. YZH helped design the biotin assays. FRR, JBL, and YZH analyzed the data. JBL wrote the manuscript. All authors edited and approved the final manuscript.
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Ren, FR., Sun, X., Wang, TY. et al. Biotin provisioning by horizontally transferred genes from bacteria confers animal fitness benefits. ISME J 14, 2542–2553 (2020). https://doi.org/10.1038/s41396-020-0704-5
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DOI: https://doi.org/10.1038/s41396-020-0704-5
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