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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...
Autores principales: | , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2021
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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. |
format | Online Article Text |
id | pubmed-8549721 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
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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