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Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions
BACKGROUND: Salmonella enterica possess several iron acquisition systems, encoded on the chromosome and plasmids. Recently, we demonstrated that incompatibility group (Inc) FIB plasmid-encoded iron acquisition systems (Sit and aerobactin) likely play an important role in persistence of Salmonella in...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6567447/ https://www.ncbi.nlm.nih.gov/pubmed/31195964 http://dx.doi.org/10.1186/s12864-019-5768-0 |
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author | Khajanchi, Bijay K. Xu, Joshua Grim, Christopher J. Ottesen, Andrea R. Ramachandran, Padmini Foley, Steven L. |
author_facet | Khajanchi, Bijay K. Xu, Joshua Grim, Christopher J. Ottesen, Andrea R. Ramachandran, Padmini Foley, Steven L. |
author_sort | Khajanchi, Bijay K. |
collection | PubMed |
description | BACKGROUND: Salmonella enterica possess several iron acquisition systems, encoded on the chromosome and plasmids. Recently, we demonstrated that incompatibility group (Inc) FIB plasmid-encoded iron acquisition systems (Sit and aerobactin) likely play an important role in persistence of Salmonella in human intestinal epithelial cells (Caco-2). In this study, we sought to determine global transcriptome analyses of S. enterica in iron-rich (IR) and iron-depleted (ID) growth conditions. RESULTS: The number of differentially-expressed genes were substantially higher for recipient (SE819) (n = 966) and transconjugant (TC) (n = 945) compared to the wild type (WT) (SE163A) (n = 110) strain in ID as compared to IR growth conditions. Several virulence-associated factors including T3SS, flagellin, cold-shock protein (cspE), and regulatory genes were upregulated in TC in ID compared to IR conditions. Whereas, IS1 and acrR/tetR transposases located on the IncFIB plasmid, ferritin and several regulatory genes were downregulated in TC in ID conditions. Enterobactin transporter (entS), iron ABC transporter (fepCD), colicin transporter, IncFIB-encoded enolase, cyclic di-GMP regulator (cdgR) and other regulatory genes of the WT strain were upregulated in ID compared to IR conditions. Conversely, ferritin, ferrous iron transport protein A (feoA), IncFIB-encoded IS1 and acrR/tetR transposases and ArtA toxin of WT were downregulated in ID conditions. SDS-PAGE coupled with LC-MS/MS analyses revealed that siderophore receptor proteins such as chromosomally-encoded IroN and, IncFIB-encoded IutA were upregulated in WT and TC in ID growth conditions. Both chromosome and IncFIB plasmid-encoded SitA was overexpressed in WT, but not in TC or recipient in ID conditions. Increased expression of flagellin was detected in recipient and TC, but not in WT in ID conditions. CONCLUSION: Iron concentrations in growth media influenced differential gene expressions both at transcriptional and translational levels, including genes encoded on the IncFIB plasmid. Limited iron availability within the host may promote pathogenic Salmonella to differentially express subsets of genes encoded by chromosome and/or plasmids, facilitating establishment of successful infection. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5768-0) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6567447 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-65674472019-06-17 Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions Khajanchi, Bijay K. Xu, Joshua Grim, Christopher J. Ottesen, Andrea R. Ramachandran, Padmini Foley, Steven L. BMC Genomics Research Article BACKGROUND: Salmonella enterica possess several iron acquisition systems, encoded on the chromosome and plasmids. Recently, we demonstrated that incompatibility group (Inc) FIB plasmid-encoded iron acquisition systems (Sit and aerobactin) likely play an important role in persistence of Salmonella in human intestinal epithelial cells (Caco-2). In this study, we sought to determine global transcriptome analyses of S. enterica in iron-rich (IR) and iron-depleted (ID) growth conditions. RESULTS: The number of differentially-expressed genes were substantially higher for recipient (SE819) (n = 966) and transconjugant (TC) (n = 945) compared to the wild type (WT) (SE163A) (n = 110) strain in ID as compared to IR growth conditions. Several virulence-associated factors including T3SS, flagellin, cold-shock protein (cspE), and regulatory genes were upregulated in TC in ID compared to IR conditions. Whereas, IS1 and acrR/tetR transposases located on the IncFIB plasmid, ferritin and several regulatory genes were downregulated in TC in ID conditions. Enterobactin transporter (entS), iron ABC transporter (fepCD), colicin transporter, IncFIB-encoded enolase, cyclic di-GMP regulator (cdgR) and other regulatory genes of the WT strain were upregulated in ID compared to IR conditions. Conversely, ferritin, ferrous iron transport protein A (feoA), IncFIB-encoded IS1 and acrR/tetR transposases and ArtA toxin of WT were downregulated in ID conditions. SDS-PAGE coupled with LC-MS/MS analyses revealed that siderophore receptor proteins such as chromosomally-encoded IroN and, IncFIB-encoded IutA were upregulated in WT and TC in ID growth conditions. Both chromosome and IncFIB plasmid-encoded SitA was overexpressed in WT, but not in TC or recipient in ID conditions. Increased expression of flagellin was detected in recipient and TC, but not in WT in ID conditions. CONCLUSION: Iron concentrations in growth media influenced differential gene expressions both at transcriptional and translational levels, including genes encoded on the IncFIB plasmid. Limited iron availability within the host may promote pathogenic Salmonella to differentially express subsets of genes encoded by chromosome and/or plasmids, facilitating establishment of successful infection. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5768-0) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-13 /pmc/articles/PMC6567447/ /pubmed/31195964 http://dx.doi.org/10.1186/s12864-019-5768-0 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. |
spellingShingle | Research Article Khajanchi, Bijay K. Xu, Joshua Grim, Christopher J. Ottesen, Andrea R. Ramachandran, Padmini Foley, Steven L. Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions |
title | Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions |
title_full | Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions |
title_fullStr | Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions |
title_full_unstemmed | Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions |
title_short | Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions |
title_sort | global transcriptomic analyses of salmonella enterica in iron-depleted and iron-rich growth conditions |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6567447/ https://www.ncbi.nlm.nih.gov/pubmed/31195964 http://dx.doi.org/10.1186/s12864-019-5768-0 |
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