학술논문

Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts.
Document Type
Article
Source
PLoS Pathogens. 11/29/2021, Vol. 17 Issue 11, p1-23. 23p.
Subject
*ESSENTIAL amino acids
*LYSINE
*ALEYRODIDAE
*AMINO acid synthesis
*SWEETPOTATO whitefly
*HORIZONTAL gene transfer
Language
ISSN
1553-7366
Abstract
Horizontal gene transfer is widespread in insects bearing intracellular symbionts. Horizontally transferred genes (HTGs) are presumably involved in amino acid synthesis in sternorrhynchan insects. However, their role in insect-symbiont interactions remains largely unknown. We found symbionts Portiera, Hamiltonella and Rickettsia possess most genes involved in lysine synthesis in the whitefly Bemisia tabaci MEAM1 although their genomes are reduced. Hamiltonella maintains a nearly complete lysine synthesis pathway. In contrast, Portiera and Rickettsia require the complementation of whitefly HTGs for lysine synthesis and have lysE, encoding a lysine exporter. Furthermore, each horizontally transferred lysine gene of ten B. tabaci cryptic species shares an evolutionary origin. We demonstrated that Hamiltonella did not alter the titers of Portiera and Rickettsia or lysine gene expression of Portiera, Rickettsia and whiteflies. Hamiltonella also did not impact on lysine levels or protein localization in bacteriocytes harboring Portiera and ovaries infected with Rickettsia. Complementation with whitefly lysine synthesis HTGs rescued E. coli lysine gene knockout mutants. Silencing whitefly lysA in whiteflies harboring Hamiltonella reduced lysine levels, adult fecundity and titers of Portiera and Rickettsia without influencing the expression of Hamiltonella lysA. Furthermore, silencing whitefly lysA in whiteflies lacking Hamiltonella reduced lysine levels, adult fecundity and titers of Portiera and Rickettsia in ovarioles. Therefore, we, for the first time, demonstrated an essential amino acid lysine synthesized through HTGs is important for whitefly reproduction and fitness of both obligate and facultative symbionts, and it illustrates the mutual dependence between whitefly and its two symbionts. Collectively, this study reveals that acquisition of horizontally transferred lysine genes contributes to coadaptation and coevolution between B. tabaci and its symbionts. Author summary: Revealing which molecules are exchanged between host and symbionts will illuminate how host and bacterial symbiont establish beneficial relationships. Horizontally transferred genes (HTGs) presumably complement the missing genes involved in synthesis of essential amino acids (EAAs) in symbionts of sternorrhynchan insects. We demonstrate that whitefly HTGs can cooperate with Portiera and Rickettsia for lysine synthesis. The lysine synthesized through HTGs impacts both whitefly reproduction and symbiont fitness. Taken together, we reveal that horizontally acquired lysine genes underlie the basis for the mutual dependence between whitefly and two intracellular symbionts. Therefore, our study demonstrates the critical role of HTGs in the synthesis of EAAs and their function in insect-symbiont interactions and coevolution. [ABSTRACT FROM AUTHOR]