Cargando…

Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer

Iron is essential for most bacteria to survive, but excessive iron leads to damage by the Fenton reaction. Therefore, the concentration of intracellular free iron must be strictly controlled in bacteria. Riemerella anatipestifer (R. anatipestifer), a Gram-negative bacterium, encodes the iron uptake...

Descripción completa

Detalles Bibliográficos
Autores principales: Huang, Mi, Liu, Mafeng, Liu, Jiajun, Zhu, Dekang, Tang, Qianying, Jia, Renyong, Chen, Shun, Zhao, Xinxin, Yang, Qiao, Wu, Ying, Zhang, Shaqiu, Huang, Juan, Ou, Xumin, Mao, Sai, Gao, Qun, Sun, Di, Wang, Mingshu, Cheng, Anchun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7976709/
https://www.ncbi.nlm.nih.gov/pubmed/33741064
http://dx.doi.org/10.1186/s13567-021-00919-9
_version_ 1783667050295590912
author Huang, Mi
Liu, Mafeng
Liu, Jiajun
Zhu, Dekang
Tang, Qianying
Jia, Renyong
Chen, Shun
Zhao, Xinxin
Yang, Qiao
Wu, Ying
Zhang, Shaqiu
Huang, Juan
Ou, Xumin
Mao, Sai
Gao, Qun
Sun, Di
Wang, Mingshu
Cheng, Anchun
author_facet Huang, Mi
Liu, Mafeng
Liu, Jiajun
Zhu, Dekang
Tang, Qianying
Jia, Renyong
Chen, Shun
Zhao, Xinxin
Yang, Qiao
Wu, Ying
Zhang, Shaqiu
Huang, Juan
Ou, Xumin
Mao, Sai
Gao, Qun
Sun, Di
Wang, Mingshu
Cheng, Anchun
author_sort Huang, Mi
collection PubMed
description Iron is essential for most bacteria to survive, but excessive iron leads to damage by the Fenton reaction. Therefore, the concentration of intracellular free iron must be strictly controlled in bacteria. Riemerella anatipestifer (R. anatipestifer), a Gram-negative bacterium, encodes the iron uptake system. However, the iron homeostasis mechanism remains largely unknown. In this study, it was shown that compared with the wild type R. anatipestifer CH-1, R. anatipestifer CH-1Δfur was more sensitive to streptonigrin, and this effect was alleviated when the bacteria were cultured in iron-depleted medium, suggesting that the fur mutant led to excess iron accumulation inside cells. Similarly, compared with R. anatipestifer CH-1∆recA, R. anatipestifer CH-1∆recAΔfur was more sensitive to H(2)O(2)-induced oxidative stress when the bacteria were grown in iron-rich medium rather than iron-depleted medium. Accordingly, it was shown that R. anatipestifer CH-1∆recAΔfur produced more intracellular ROS than R. anatipestifer CH-1∆recA in iron-rich medium. Electrophoretic mobility shift assays showed that R. anatipestifer CH-1 Fur suppressed the transcription of putative iron uptake genes through binding to their promoter regions. Finally, it was shown that compared with the wild type, R. anatipestifer CH-1Δfur was significantly attenuated in ducklings and that the colonization ability of R. anatipestifer CH-1Δfur in various tissues or organs was decreased. All these results suggested that Fur is important for iron homeostasis in R. anatipestifer and its pathogenic mechanism. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-021-00919-9.
format Online
Article
Text
id pubmed-7976709
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-79767092021-03-19 Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer Huang, Mi Liu, Mafeng Liu, Jiajun Zhu, Dekang Tang, Qianying Jia, Renyong Chen, Shun Zhao, Xinxin Yang, Qiao Wu, Ying Zhang, Shaqiu Huang, Juan Ou, Xumin Mao, Sai Gao, Qun Sun, Di Wang, Mingshu Cheng, Anchun Vet Res Research Article Iron is essential for most bacteria to survive, but excessive iron leads to damage by the Fenton reaction. Therefore, the concentration of intracellular free iron must be strictly controlled in bacteria. Riemerella anatipestifer (R. anatipestifer), a Gram-negative bacterium, encodes the iron uptake system. However, the iron homeostasis mechanism remains largely unknown. In this study, it was shown that compared with the wild type R. anatipestifer CH-1, R. anatipestifer CH-1Δfur was more sensitive to streptonigrin, and this effect was alleviated when the bacteria were cultured in iron-depleted medium, suggesting that the fur mutant led to excess iron accumulation inside cells. Similarly, compared with R. anatipestifer CH-1∆recA, R. anatipestifer CH-1∆recAΔfur was more sensitive to H(2)O(2)-induced oxidative stress when the bacteria were grown in iron-rich medium rather than iron-depleted medium. Accordingly, it was shown that R. anatipestifer CH-1∆recAΔfur produced more intracellular ROS than R. anatipestifer CH-1∆recA in iron-rich medium. Electrophoretic mobility shift assays showed that R. anatipestifer CH-1 Fur suppressed the transcription of putative iron uptake genes through binding to their promoter regions. Finally, it was shown that compared with the wild type, R. anatipestifer CH-1Δfur was significantly attenuated in ducklings and that the colonization ability of R. anatipestifer CH-1Δfur in various tissues or organs was decreased. All these results suggested that Fur is important for iron homeostasis in R. anatipestifer and its pathogenic mechanism. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13567-021-00919-9. BioMed Central 2021-03-19 2021 /pmc/articles/PMC7976709/ /pubmed/33741064 http://dx.doi.org/10.1186/s13567-021-00919-9 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Huang, Mi
Liu, Mafeng
Liu, Jiajun
Zhu, Dekang
Tang, Qianying
Jia, Renyong
Chen, Shun
Zhao, Xinxin
Yang, Qiao
Wu, Ying
Zhang, Shaqiu
Huang, Juan
Ou, Xumin
Mao, Sai
Gao, Qun
Sun, Di
Wang, Mingshu
Cheng, Anchun
Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer
title Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer
title_full Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer
title_fullStr Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer
title_full_unstemmed Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer
title_short Functional characterization of Fur in iron metabolism, oxidative stress resistance and virulence of Riemerella anatipestifer
title_sort functional characterization of fur in iron metabolism, oxidative stress resistance and virulence of riemerella anatipestifer
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7976709/
https://www.ncbi.nlm.nih.gov/pubmed/33741064
http://dx.doi.org/10.1186/s13567-021-00919-9
work_keys_str_mv AT huangmi functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT liumafeng functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT liujiajun functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT zhudekang functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT tangqianying functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT jiarenyong functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT chenshun functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT zhaoxinxin functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT yangqiao functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT wuying functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT zhangshaqiu functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT huangjuan functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT ouxumin functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT maosai functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT gaoqun functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT sundi functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT wangmingshu functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer
AT chenganchun functionalcharacterizationoffurinironmetabolismoxidativestressresistanceandvirulenceofriemerellaanatipestifer