Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts

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.

A novel microRNA regulates cooperation between symbiont and a laterally acquired gene in the regulation of pantothenate biosynthesis within Bemisia tabaci whiteflies

“…Some HTGs or their encoded proteins are highly expressed in insect bacteriocytes (Bao et al, 2021;Husnik et al, 2013;Luan et al, 2015;Moran & Bennett, 2014;Ren et al, 2021;Sloan et al, 2014). (Chen et al, 2016).…”

“…Some HTGs or their encoded proteins are highly expressed in insect bacteriocytes (Bao et al, 2021; Husnik et al, 2013; Luan et al, 2015; Moran & Bennett, 2014; Ren et al, 2021; Sloan et al, 2014). However, the means by which the expression of host HTGs or their proteins is regulated, and thereby impact host–symbiont interactions, remain unknown.…”

“…Total RNA was extracted as previously described (Ren et al, 2020). cDNAs were synthesized from the total RNA using an All‐in‐One cDNA Synthesis SuperMix Kit (Bimake) as previously described (Bao et al, 2021; Ren et al, 2021). The qRT‐PCRs were performed using the CFX96 Real‐Time PCR Detection System (Bio‐Rad) with 2×SYBR Green master Mix (Bimake).…”

“…The miRNA antagomir is the chemically modified single‐stranded miRNA that complements the miRNAs and can specifically silence the endogenous miRNAs (Krutzfeldt et al, 2005). To investigate whether overexpression or repression of novel‐m0780‐5p influences PanBC localization in whiteflies, ~800 female adult whiteflies infected with Portiera within 3–4 days after emergence were injected with 3 µ m agomir or antagomir using an Eppendorf microinjection system following a previously described method (Bao et al, 2021; Li et al, 2022; Ren et al, 2021; Wang et al, 2022). The whiteflies that were injected with 3 µ m negative control agomir were used as a negative control for agomir injection.…”

“…In one such instance, horizontally transferred murF collaborates with the symbiont Moranella for peptidoglycan synthesis in mealybugs (Bublitz et al, 2019). Laterally transferred lysA cooperates with the symbionts Portiera and Rickettsia for lysine synthesis in whiteflies (Bao et al, 2021). Similarly, and of relevance to our study, the horizontally acquired panBC gene cooperates with the symbiont Portiera for pantothenate synthesis in whiteflies (Ren et al, 2021).…”