Global transcriptomic analyses of Salmonella enterica in Iron-depleted and Iron-rich growth conditions

Bijay K Khajanchi,Joshua Xu,Steven L Foley,Andrea R Ottesen,Padmini Ramachandran,Christopher J Grim

doi:10.1186/s12864-019-5768-0

Abstract

BackgroundSalmonella 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.ResultsThe 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.ConclusionIron 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.

Highlights

Salmonella enterica possess several iron acquisition systems, encoded on the chromosome and plasmids
We demonstrated that Incompatibility group FIB plasmid (IncFIB) plasmid-encoded iron acquisition systems (Sit and aerobactin) likely play an important role in persistence of Salmonella in human intestinal epithelial cells [18]
To determine influence of iron on the transcriptomes of wild type (WT) (SE163A), transconjugant (TC) (SE819::IncFIB) and recipient (SE819) Salmonella enterica strains, RNA-Seq analyses were performed using RNA extracted from these strains in IR and ID growth conditions

Summary

Introduction

Salmonella enterica possess several iron acquisition systems, encoded on the chromosome and plasmids. 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). Over 2600 Salmonella serovars have been identified, largely differing in host ranges and their ability to cause human infections [5]. Salmonella enterica serovars such as Enteritidis, Typhimurium, Newport, and Heidelberg can colonize intestines of a broad range of hosts including food producing animals and humans [6]. Genetic factors that contribute to boarder host range and increased ability to cause invasive form of disease to different Salmonella serovars are still largely unknown

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