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A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola

Iron is an essential element for the growth and survival of pathogenic bacteria; however, it is not fully understood how bacteria sense and respond to iron deficiency or excess. In this study, we show that xfeA in Xanthomonas oryzae pv. oryzicola senses extracytoplasmic iron and changes the hydrogen...

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Autores principales: Nie, Wenhan, Wang, Sai, Huang, Jin, Xu, Qin, Wang, Peihong, Wu, Yan, He, Rui, Yiming, Ayizekeranmu, Liang, Jingling, Ahmad, Iftikhar, Fu, Luoyi, Guo, Longbiao, Yuan, Junhua, Zhu, Bo, Chen, Gongyou
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549721/
https://www.ncbi.nlm.nih.gov/pubmed/34704802
http://dx.doi.org/10.1128/Spectrum.01571-21
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author Nie, Wenhan
Wang, Sai
Huang, Jin
Xu, Qin
Wang, Peihong
Wu, Yan
He, Rui
Yiming, Ayizekeranmu
Liang, Jingling
Ahmad, Iftikhar
Fu, Luoyi
Guo, Longbiao
Yuan, Junhua
Zhu, Bo
Chen, Gongyou
author_facet Nie, Wenhan
Wang, Sai
Huang, Jin
Xu, Qin
Wang, Peihong
Wu, Yan
He, Rui
Yiming, Ayizekeranmu
Liang, Jingling
Ahmad, Iftikhar
Fu, Luoyi
Guo, Longbiao
Yuan, Junhua
Zhu, Bo
Chen, Gongyou
author_sort Nie, Wenhan
collection PubMed
description Iron is an essential element for the growth and survival of pathogenic bacteria; however, it is not fully understood how bacteria sense and respond to iron deficiency or excess. In this study, we show that xfeA in Xanthomonas oryzae pv. oryzicola senses extracytoplasmic iron and changes the hydrogen bonding network of ligand channel domains by adenosine-to-inosine (A-to-I) RNA editing. The frequency of A-to-I RNA editing during iron-deficient conditions increased by 76.87%, which facilitated the passage of iron through the XfeA outer membrane channel. When bacteria were subjected to high iron concentrations, the percentage of A-to-I editing in xfeA decreased, which reduced iron transport via XfeA. Furthermore, A-to-I RNA editing increased expression of multiple genes in the chemotaxis pathway, including methyl-accepting chemotaxis proteins (MCPs) that sense concentrations of exogenous ferrienterobactin (Fe-Ent) at the cytoplasmic membrane. A-to-I RNA editing helps X. oryzae pv. oryzicola move toward an iron-rich environment and supports our contention that editing in xfeA facilitates entry of a ferric siderophore. Overall, our results reveal a new signaling mechanism that bacteria use to adjust to iron concentrations. IMPORTANCE Adenosine-to-inosine (A-to-I) RNA editing, which is catalyzed by the adenosine deaminase RNA-specific family of enzymes, is a frequent posttranscriptional modification in metazoans. Research on A-to-I editing in bacteria is limited, and the importance of this editing is underestimated. In this study, we show that bacteria may use A-to-I editing as an alternative strategy to promote uptake of metabolic iron, and this form of editing can quickly and precisely modify RNA and subsequent protein sequences similar to an “on/off” switch. Thus, bacteria have the capacity to use a rapid switch-like mechanism to facilitate iron uptake and improve their competitiveness.
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spelling pubmed-85497212021-11-08 A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola Nie, Wenhan Wang, Sai Huang, Jin Xu, Qin Wang, Peihong Wu, Yan He, Rui Yiming, Ayizekeranmu Liang, Jingling Ahmad, Iftikhar Fu, Luoyi Guo, Longbiao Yuan, Junhua Zhu, Bo Chen, Gongyou Microbiol Spectr Research Article Iron is an essential element for the growth and survival of pathogenic bacteria; however, it is not fully understood how bacteria sense and respond to iron deficiency or excess. In this study, we show that xfeA in Xanthomonas oryzae pv. oryzicola senses extracytoplasmic iron and changes the hydrogen bonding network of ligand channel domains by adenosine-to-inosine (A-to-I) RNA editing. The frequency of A-to-I RNA editing during iron-deficient conditions increased by 76.87%, which facilitated the passage of iron through the XfeA outer membrane channel. When bacteria were subjected to high iron concentrations, the percentage of A-to-I editing in xfeA decreased, which reduced iron transport via XfeA. Furthermore, A-to-I RNA editing increased expression of multiple genes in the chemotaxis pathway, including methyl-accepting chemotaxis proteins (MCPs) that sense concentrations of exogenous ferrienterobactin (Fe-Ent) at the cytoplasmic membrane. A-to-I RNA editing helps X. oryzae pv. oryzicola move toward an iron-rich environment and supports our contention that editing in xfeA facilitates entry of a ferric siderophore. Overall, our results reveal a new signaling mechanism that bacteria use to adjust to iron concentrations. IMPORTANCE Adenosine-to-inosine (A-to-I) RNA editing, which is catalyzed by the adenosine deaminase RNA-specific family of enzymes, is a frequent posttranscriptional modification in metazoans. Research on A-to-I editing in bacteria is limited, and the importance of this editing is underestimated. In this study, we show that bacteria may use A-to-I editing as an alternative strategy to promote uptake of metabolic iron, and this form of editing can quickly and precisely modify RNA and subsequent protein sequences similar to an “on/off” switch. Thus, bacteria have the capacity to use a rapid switch-like mechanism to facilitate iron uptake and improve their competitiveness. American Society for Microbiology 2021-10-27 /pmc/articles/PMC8549721/ /pubmed/34704802 http://dx.doi.org/10.1128/Spectrum.01571-21 Text en Copyright © 2021 Nie et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Nie, Wenhan
Wang, Sai
Huang, Jin
Xu, Qin
Wang, Peihong
Wu, Yan
He, Rui
Yiming, Ayizekeranmu
Liang, Jingling
Ahmad, Iftikhar
Fu, Luoyi
Guo, Longbiao
Yuan, Junhua
Zhu, Bo
Chen, Gongyou
A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola
title A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola
title_full A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola
title_fullStr A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola
title_full_unstemmed A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola
title_short A-to-I mRNA Editing in a Ferric Siderophore Receptor Improves Competition for Iron in Xanthomonas oryzae pv. oryzicola
title_sort a-to-i mrna editing in a ferric siderophore receptor improves competition for iron in xanthomonas oryzae pv. oryzicola
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549721/
https://www.ncbi.nlm.nih.gov/pubmed/34704802
http://dx.doi.org/10.1128/Spectrum.01571-21
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