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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...

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Autores principales: Khajanchi, Bijay K., Xu, Joshua, Grim, Christopher J., Ottesen, Andrea R., Ramachandran, Padmini, Foley, Steven L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
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.
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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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