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The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia
BACKGROUND: Stenotrophomonas maltophilia, a member of γ-proteobacteria, is a ubiquitous environmental bacterium that is recognized as an opportunistic nosocomial pathogen. FecABCD system contributes to ferric citrate acquisition in Escherichia coli. FeoABC system, consisting of an inner membrane tra...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2022
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9047314/ https://www.ncbi.nlm.nih.gov/pubmed/35477574 http://dx.doi.org/10.1186/s12929-022-00809-y |
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author | Liao, Chun-Hsing Lu, Hsu-Feng Huang, Hsin-Hui Chen, Yu Li, Li-Hua Lin, Yi-Tsung Yang, Tsuey-Ching |
author_facet | Liao, Chun-Hsing Lu, Hsu-Feng Huang, Hsin-Hui Chen, Yu Li, Li-Hua Lin, Yi-Tsung Yang, Tsuey-Ching |
author_sort | Liao, Chun-Hsing |
collection | PubMed |
description | BACKGROUND: Stenotrophomonas maltophilia, a member of γ-proteobacteria, is a ubiquitous environmental bacterium that is recognized as an opportunistic nosocomial pathogen. FecABCD system contributes to ferric citrate acquisition in Escherichia coli. FeoABC system, consisting of an inner membrane transporter (FeoB) and two cytoplasmic proteins (FeoA and FeoC), is a well-known ferrous iron transporter system in γ-proteobacteria. As revealed by the sequenced genome, S. maltophilia appears to be equipped with several iron acquisition systems; however, the understanding of these systems is limited. In this study, we aimed to elucidate the ferric citrate acquisition system of S. maltophilia. METHODS: Candidate genes searching and function validation are the strategy for elucidating the genes involved in ferric citrate acquisition. The candidate genes responsible for ferric citrate acquisition were firstly selected using FecABCD of E. coli as a reference, and then revealed by transcriptome analysis of S. maltophilia KJ with and without 2,2′-dipyridyl (DIP) treatment. Function validation was carried out by deletion mutant construction and ferric citrate utilization assay. The bacterial adenylate cyclase two-hybrid system was used to verify intra-membrane protein–protein interaction. RESULTS: Smlt2858 and Smlt2356, the homologues of FecA and FecC/D of E. coli, were first considered; however, deletion mutant construction and functional validation ruled out their involvement in ferric citrate acquisition. FciA (Smlt1148), revealed by its upregulation in DIP-treated KJ cells, was the outer membrane receptor for ferric citrate uptake. The fciA gene is a member of the fciTABC operon, in which fciT, fciA, and fciC participated in ferric citrate acquisition. Uniquely, the Feo system of S. maltophilia is composed of a cytoplasmic protein FeoA, an inner membrane transporter FeoB, and a predicted inner membrane protein FeoI. The intra-membrane protein–protein interaction between FeoB and FeoI may extend the substrate profile of FeoB to ferric citrate. FeoABI system functioned as an inner membrane transporter of ferric citrate. CONCLUSIONS: The FciTABC and FeoABI systems contribute to ferric citrate acquisition in S. maltophilia. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12929-022-00809-y. |
format | Online Article Text |
id | pubmed-9047314 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-90473142022-04-29 The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia Liao, Chun-Hsing Lu, Hsu-Feng Huang, Hsin-Hui Chen, Yu Li, Li-Hua Lin, Yi-Tsung Yang, Tsuey-Ching J Biomed Sci Research BACKGROUND: Stenotrophomonas maltophilia, a member of γ-proteobacteria, is a ubiquitous environmental bacterium that is recognized as an opportunistic nosocomial pathogen. FecABCD system contributes to ferric citrate acquisition in Escherichia coli. FeoABC system, consisting of an inner membrane transporter (FeoB) and two cytoplasmic proteins (FeoA and FeoC), is a well-known ferrous iron transporter system in γ-proteobacteria. As revealed by the sequenced genome, S. maltophilia appears to be equipped with several iron acquisition systems; however, the understanding of these systems is limited. In this study, we aimed to elucidate the ferric citrate acquisition system of S. maltophilia. METHODS: Candidate genes searching and function validation are the strategy for elucidating the genes involved in ferric citrate acquisition. The candidate genes responsible for ferric citrate acquisition were firstly selected using FecABCD of E. coli as a reference, and then revealed by transcriptome analysis of S. maltophilia KJ with and without 2,2′-dipyridyl (DIP) treatment. Function validation was carried out by deletion mutant construction and ferric citrate utilization assay. The bacterial adenylate cyclase two-hybrid system was used to verify intra-membrane protein–protein interaction. RESULTS: Smlt2858 and Smlt2356, the homologues of FecA and FecC/D of E. coli, were first considered; however, deletion mutant construction and functional validation ruled out their involvement in ferric citrate acquisition. FciA (Smlt1148), revealed by its upregulation in DIP-treated KJ cells, was the outer membrane receptor for ferric citrate uptake. The fciA gene is a member of the fciTABC operon, in which fciT, fciA, and fciC participated in ferric citrate acquisition. Uniquely, the Feo system of S. maltophilia is composed of a cytoplasmic protein FeoA, an inner membrane transporter FeoB, and a predicted inner membrane protein FeoI. The intra-membrane protein–protein interaction between FeoB and FeoI may extend the substrate profile of FeoB to ferric citrate. FeoABI system functioned as an inner membrane transporter of ferric citrate. CONCLUSIONS: The FciTABC and FeoABI systems contribute to ferric citrate acquisition in S. maltophilia. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12929-022-00809-y. BioMed Central 2022-04-27 /pmc/articles/PMC9047314/ /pubmed/35477574 http://dx.doi.org/10.1186/s12929-022-00809-y Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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 Liao, Chun-Hsing Lu, Hsu-Feng Huang, Hsin-Hui Chen, Yu Li, Li-Hua Lin, Yi-Tsung Yang, Tsuey-Ching The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia |
title | The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia |
title_full | The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia |
title_fullStr | The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia |
title_full_unstemmed | The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia |
title_short | The fciTABC and feoABI systems contribute to ferric citrate acquisition in Stenotrophomonas maltophilia |
title_sort | fcitabc and feoabi systems contribute to ferric citrate acquisition in stenotrophomonas maltophilia |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9047314/ https://www.ncbi.nlm.nih.gov/pubmed/35477574 http://dx.doi.org/10.1186/s12929-022-00809-y |
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