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PMID: 15231804 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Iron acquisition and regulation in Campylobacter jejuni.

Journal of bacteriology ·Vol. 186 ·No. 14 ·2004-07-00 ·Pages 4714-29

Palyada K, Threadgill D, Stintzi A

Abstract

Iron affects the physiology of bacteria in two different ways: as a micronutrient for bacterial growth and as a catalyst for the formation of hydroxyl radicals. In this study, we used DNA microarrays to identify the C. jejuni genes that have their transcript abundance affected by iron availability. The transcript levels of 647 genes were affected after the addition of iron to iron-limited C. jejuni cells. Several classes of affected genes were revealed within 15 min, including immediate-early response genes as well as those specific to iron acquisition and metabolism. In contrast, only 208 genes were differentially expressed during steady-state experiments comparing iron-rich and iron-limited growth conditions. As expected, genes annotated as being involved in either iron acquisition or oxidative stress defense were downregulated during both time course and steady-state experiments, while genes encoding proteins involved in energy metabolism were upregulated. Because the level of protein glycosylation increased with iron limitation, iron may modulate the level of C. jejuni virulence by affecting the degree of protein glycosylation. Since iron homeostasis has been shown to be Fur regulated in C. jejuni, an isogenic fur mutant was used to define the Fur regulon by transcriptome profiling. A total of 53 genes were Fur regulated, including many genes not previously associated with Fur regulation. A putative Fur binding consensus sequence was identified in the promoter region of most iron-repressed and Fur-regulated genes. Interestingly, a fur mutant was found to be significantly affected in its ability to colonize the gastrointestinal tract of chicks, highlighting the importance of iron homeostasis in vivo. Directed mutagenesis of other genes identified by the microarray analyses allowed the characterization of the ferric enterobactin receptor, previously named CfrA. Chick colonization assays indicated that mutants defective in enterobactin-mediated iron acquisition were unable to colonize the gastrointestinal tract. In addition, a mutation in a receptor (Cj0178) for an uncharacterized iron source also resulted in reduced colonization potential. Overall, this work documents the complex response of C. jejuni to iron availability, describes the genetic network between the Fur and iron regulons, and provides insight regarding the role of iron in C. jejuni colonization in vivo.

MeSH Terms
Adaptation, Physiological Animals Bacterial Outer Membrane Proteins/genetics,physiology Bacterial Proteins/genetics,physiology Campylobacter Infections/microbiology Campylobacter jejuni/genetics,growth & development,metabolism,pathogenicity Carrier Proteins/genetics,physiology Chickens/microbiology Conserved Sequence Gene Deletion Gene Expression Profiling Gene Expression Regulation, Bacterial Genes, Bacterial Glycosylation Iron/metabolism Mutation Oligonucleotide Array Sequence Analysis Operon Oxidative Stress Promoter Regions, Genetic Receptors, Cell Surface/genetics,physiology Regulon Repressor Proteins/genetics,physiology Virulence
Chemicals
Bacterial Outer Membrane Proteins Bacterial Proteins Carrier Proteins Receptors, Cell Surface Repressor Proteins enterobactin receptor ferric uptake regulating proteins, bacterial Iron
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Palyada Kiran
Department of Veterinary Pathobiology, College of Veterinary Medicine, Oklahoma State University, Stillwater, OK 74078, USA.
Threadgill Deborah
Stintzi Alain
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Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2004-07-00
Pages
4714-29
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC438614
Subset
IM
Grants
NCRR NIH HHS · P20 RR015564 · United States
NIAID NIH HHS · R01 AI055612 · United States
NIAID NIH HHS · R01-AI055612 · United States
NCRR NIH HHS · RR15564 · United States
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