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

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 Portier...

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Autores principales: Bao, Xi-Yu, Yan, Jin-Yang, Yao, Ya-Lin, Wang, Yan-Bin, Visendi, Paul, Seal, Susan, Luan, Jun-Bo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8659303/
https://www.ncbi.nlm.nih.gov/pubmed/34843593
http://dx.doi.org/10.1371/journal.ppat.1010120
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author Bao, Xi-Yu
Yan, Jin-Yang
Yao, Ya-Lin
Wang, Yan-Bin
Visendi, Paul
Seal, Susan
Luan, Jun-Bo
author_facet Bao, Xi-Yu
Yan, Jin-Yang
Yao, Ya-Lin
Wang, Yan-Bin
Visendi, Paul
Seal, Susan
Luan, Jun-Bo
author_sort Bao, Xi-Yu
collection PubMed
description 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.
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spelling pubmed-86593032021-12-10 Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts Bao, Xi-Yu Yan, Jin-Yang Yao, Ya-Lin Wang, Yan-Bin Visendi, Paul Seal, Susan Luan, Jun-Bo PLoS Pathog Research Article 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. Public Library of Science 2021-11-29 /pmc/articles/PMC8659303/ /pubmed/34843593 http://dx.doi.org/10.1371/journal.ppat.1010120 Text en © 2021 Bao et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Bao, Xi-Yu
Yan, Jin-Yang
Yao, Ya-Lin
Wang, Yan-Bin
Visendi, Paul
Seal, Susan
Luan, Jun-Bo
Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts
title Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts
title_full Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts
title_fullStr Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts
title_full_unstemmed Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts
title_short Lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts
title_sort lysine provisioning by horizontally acquired genes promotes mutual dependence between whitefly and two intracellular symbionts
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8659303/
https://www.ncbi.nlm.nih.gov/pubmed/34843593
http://dx.doi.org/10.1371/journal.ppat.1010120
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