Intracellular symbionts in insects often have reduced genomes. Host acquisition of genes from bacteria is an important adaptation that supports symbionts. However, the function of horizontally transferred genes in insect symbiosis remains largely unclear. The primary symbiont Portiera housed in bacteriocytes lacks pantothenate synthesis genes: panB and panC, which is presumably complemented by a fused gene panB-panC (hereafter panBC) horizontally transferred from bacteria in Bemisia tabaci MEAM1. We found panBC in many laboratory cultures, and species of B. tabaci shares a common evolutionary origin. We demonstrated that complementation with whitefly panBC rescued E. coli pantothenate gene knockout mutants. Portiera elimination decreased the pantothenate level and PanBC abundance in bacteriocytes, and reduced whitefly survival and fecundity. Silencing PanBC decreased the Portiera titer, reduced the pantothenate level, and decreased whitefly survival and fecundity. Supplementation with pantothenate restored the symbiont titer, PanBC level, and fitness of RNAi whiteflies. These data suggest that pantothenate synthesis requires cooperation and coordination of whitefly PanBC expression and Portiera. This host–symbiont co-regulation was mediated by the pantothenate level. Our findings demonstrated that pantothenate production, by the cooperation of a horizontally acquired, fused bacteria gene and Portiera, facilitates the coordination of whitefly and symbiont fitness. Thus, this study extends our understanding on the basis of complex host–symbiont interactions.
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The authors thank Professor Angela E. Douglas from Cornell University for constructive comments. We thank Professor Liu Shu-Sheng from Zhejiang University for providing the B. tabaci MEAM1 culture, and Dr Zhang De-Xian, Liu Bing-Qi, Li Ce, and Wang Yan-Bin for their assistance with the experiments. We thank Dr Zhang Xue from China Agricultural University for help and advice on E. coli functional complementation experiments. This work was supported by the National Natural Science Foundation of China (No. 31871967), High-Level Talent Support Foundation from Liaoning and Shenyang Agricultural University (Project XLYC1902104 and 880418001).
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Ren, FR., Sun, X., Wang, TY. et al. Pantothenate mediates the coordination of whitefly and symbiont fitness. ISME J (2021). https://doi.org/10.1038/s41396-020-00877-8