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.
Highlights
Microbial symbionts in insects can help them utilize food with unbalanced nutritional content by providing specific nutrients that hosts cannot synthesize [1,2,3,4,5]
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 Horizontally transferred genes (HTGs) can cooperate with Portiera and Rickettsia for lysine synthesis
Summary
Microbial symbionts in insects can help them utilize food with unbalanced nutritional content by providing specific nutrients that hosts cannot synthesize [1,2,3,4,5]. These symbionts are considered to be obligate symbionts. Other symbionts associated with insects, which may affect insect fitness under certain conditions, are called facultative symbionts [6]. Many insect symbionts are localized in the gut and hemocoel or within specialized host cells (bacteriocytes) [6]. Our understanding of insect-symbiont coadaptation is limited [7]
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