scholarly journals Complex Iron Uptake by the Putrebactin-Mediated and Feo Systems in Shewanella oneidensis

2018 ◽  
Vol 84 (20) ◽  
Author(s):  
Lulu Liu ◽  
Shisheng Li ◽  
Sijing Wang ◽  
Ziyang Dong ◽  
Haichun Gao
Keyword(s):  
Iron Uptake ◽  
Iron Homeostasis ◽  
Shewanella Oneidensis ◽  
Special Role ◽  
Uptake System ◽  
Biological Processes ◽  
Content Type ◽  
Iron Uptake System ◽  
Reducing Bacteria ◽  
Metal Reducing Bacteria

ABSTRACT Shewanella oneidensis is an extensively studied bacterium capable of respiring minerals, including a variety of iron ores, as terminal electron acceptors (EAs). Although iron plays an essential and special role in iron respiration of S. oneidensis, little has been done to date to investigate the characteristics of iron transport in this bacterium. In this study, we found that all proteins encoded by the pub-putA-putB cluster for putrebactin (S. oneidensis native siderophore) synthesis (PubABC), recognition-transport of Fe3+-putrebactin across the outer membrane (PutA), and reduction of ferric putrebactin (PutB) are essential to putrebactin-mediated iron uptake. Although homologs of PutA are many, none can function as its replacement, but some are able to work with other bacterial siderophores. We then showed that Fe2+-specific Feo is the other primary iron uptake system, based on the synthetical lethal phenotype resulting from the loss of both iron uptake routes. The role of the Feo system in iron uptake appears to be more critical, as growth is significantly impaired by the absence of the system but not of putrebactin. Furthermore, we demonstrate that hydroxyl acids, especially α-types such as lactate, promote iron uptake in a Feo-dependent manner. Overall, our findings underscore the importance of the ferrous iron uptake system in metal-reducing bacteria, providing an insight into iron homeostasis by linking these two biological processes. IMPORTANCE S. oneidensis is among the first- and the best-studied metal-reducing bacteria, with great potential in bioremediation and biotechnology. However, many questions regarding mechanisms closely associated with those applications, such as iron homeostasis, including iron uptake, export, and regulation, remain to be addressed. Here we show that Feo is a primary player in iron uptake in addition to the siderophore-dependent route. The investigation also resolved a few puzzles regarding the unexpected phenotypes of the putA mutant and lactate-dependent iron uptake. By elucidating the physiological roles of these two important iron uptake systems, this work revealed the breadth of the impacts of iron uptake systems on the biological processes.

scholarly journals Investigating theCampylobacter jejuniTranscriptional Response to Host Intestinal Extracts Reveals the Involvement of a Widely Conserved Iron Uptake System

mBio ◽  
2018 ◽  
Vol 9 (4) ◽  
Author(s):  
Martha M. Liu ◽  
Christine J. Boinett ◽  
Anson C. K. Chan ◽  
Julian Parkhill ◽  
Michael E. P. Murphy ◽  
...  
Keyword(s):  
Iron Uptake ◽  
Bacterial Species ◽  
Molecular Genetic ◽  
Uptake System ◽  
Transcriptional Responses ◽  
Susceptible Animal ◽  
Susceptible Host ◽  
Altered Expression ◽  
Content Type ◽  
Iron Uptake System

ABSTRACTCampylobacter jejuniis a pathogenic bacterium that causes gastroenteritis in humans yet is a widespread commensal in wild and domestic animals, particularly poultry. Using RNA sequencing, we assessedC. jejunitranscriptional responses to medium supplemented with human fecal versus chicken cecal extracts and in extract-supplemented medium versus medium alone.C. jejuniexposed to extracts had altered expression of 40 genes related to iron uptake, metabolism, chemotaxis, energy production, and osmotic stress response. In human fecal versus chicken cecal extracts,C. jejunidisplayed higher expression of genes involved in respiration (fdhTU) and in known or putative iron uptake systems (cfbpA,ceuB,chuC, andCJJ81176_1649–1655[here designated1649–1655]). The1649–1655genes and downstream overlapping gene1656were investigated further. Uncharacterized homologues of this system were identified in 33 diverse bacterial species representing 6 different phyla, 21 of which are associated with human disease. The1649and1650(p19) genes encode an iron transporter and a periplasmic iron binding protein, respectively; however, the role of the downstream1651–1656genes was unknown. A Δ1651–1656deletion strain had an iron-sensitive phenotype, consistent with a previously characterized Δp19mutant, and showed reduced growth in acidic medium, increased sensitivity to streptomycin, and higher resistance to H2O2stress. In iron-restricted medium, the1651–1656andp19genes were required for optimal growth when using human fecal extracts as an iron source. Collectively, this implicates a function for the1649–1656gene cluster inC. jejuniiron scavenging and stress survival in the human intestinal environment.IMPORTANCEDirect comparative studies ofC. jejuniinfection of a zoonotic commensal host and a disease-susceptible host are crucial to understanding the causes of infection outcome in humans. These studies are hampered by the lack of a disease-susceptible animal model reliably displaying a similar pathology to human campylobacteriosis. In this work, we compared the phenotypic and transcriptional responses ofC. jejunito intestinal compositions of humans (disease-susceptible host) and chickens (zoonotic host) by using human fecal and chicken cecal extracts. The mammalian gut is a complex and dynamic system containing thousands of metabolites that contribute to host health and modulate pathogen activity. We identifiedC. jejunigenes more highly expressed during exposure to human fecal extracts in comparison to chicken cecal extracts and differentially expressed in extracts compared with medium alone, and targeted one specific iron uptake system for further molecular, genetic, and phenotypic study.

scholarly journals Iron Acquisition in Mycobacterium avium subsp. paratuberculosis

2015 ◽  
Vol 198 (5) ◽  
pp. 857-866 ◽  
Author(s):  
Joyce Wang ◽  
Jalal Moolji ◽  
Alex Dufort ◽  
Alfredo Staffa ◽  
Pilar Domenech ◽  
...  
Keyword(s):  
Mycobacterium Avium ◽  
Iron Uptake ◽  
Genomic Island ◽  
Iron Acquisition ◽  
Laboratory Data ◽  
Uptake System ◽  
Intracellular Iron ◽  
Content Type ◽  
Iron Uptake System ◽  
Environmental Bacterium

ABSTRACTMycobacterium aviumsubsp.paratuberculosisis a host-adapted pathogen that evolved from the environmental bacteriumM. aviumsubsp.hominissuisthrough gene loss and gene acquisition. Growth ofM. aviumsubsp.paratuberculosisin the laboratory is enhanced by supplementation of the media with the iron-binding siderophore mycobactin J. Here we examined the production of mycobactins by related organisms and searched for an alternative iron uptake system inM. aviumsubsp.paratuberculosis. Through thin-layer chromatography and radiolabeled iron-uptake studies, we showed thatM. aviumsubsp.paratuberculosisis impaired for both mycobactin synthesis and iron acquisition. Consistent with these observations, we identified several mutations, including deletions, inM. aviumsubsp.paratuberculosisgenes coding for mycobactin synthesis. Using a transposon-mediated mutagenesis screen conditional on growth without myobactin, we identified a potential mycobactin-independent iron uptake system on aM. aviumsubsp.paratuberculosis-specific genomic island, LSPP15. We obtained a transposon (Tn) mutant with a disruption in the LSPP15 geneMAP3776cfor targeted study. The mutant manifests increased iron uptake as well as intracellular iron content, with genes downstream of the transposon insertion (MAP3775ctoMAP3772c[MAP3775-2c]) upregulated as the result of a polar effect. As an independent confirmation, we observed the same iron uptake phenotypes by overexpressingMAP3775-2cin wild-typeM. aviumsubsp.paratuberculosis. These data indicate that the horizontally acquired LSPP15 genes contribute to iron acquisition byM. aviumsubsp.paratuberculosis, potentially allowing the subsequent loss of siderophore production by this pathogen.IMPORTANCEMany microbes are able to scavenge iron from their surroundings by producing iron-chelating siderophores. One exception isMycobacterium aviumsubsp.paratuberculosis, a fastidious, slow-growing animal pathogen whose growth needs to be supported by exogenous mycobacterial siderophore (mycobactin) in the laboratory. Data presented here demonstrate that, compared to other closely relatedM. aviumsubspecies, mycobactin production and iron uptake are different inM. aviumsubsp.paratuberculosis, and these phenotypes may be caused by numerous deletions in its mycobactin biosynthesis pathway. Using a genomic approach, supplemented by targeted genetic and biochemical studies, we identified that LSPP15, a horizontally acquired genomic island, may encode an alternative iron uptake system. These findings shed light on the potential physiological consequence of horizontal gene transfer inM. aviumsubsp.paratuberculosisevolution.

scholarly journals Fur-Regulated Iron Uptake System of Edwardsiella ictaluri and Its Influence on Pathogenesis and Immunogenicity in the Catfish Host

2012 ◽  
Vol 80 (8) ◽  
pp. 2689-2703 ◽  
Author(s):  
Javier Santander ◽  
Greg Golden ◽  
Soo-Young Wanda ◽  
Roy Curtiss
Keyword(s):  
Ictalurus Punctatus ◽  
Iron Uptake ◽  
Bacterial Pathogens ◽  
Oral Vaccine ◽  
Edwardsiella Ictaluri ◽  
Uptake System ◽  
Content Type ◽  
Iron Uptake System ◽  
Fur Protein

ABSTRACTThe ability of bacterial pathogens to take up iron from the host during infection is necessary for their multiplication within the host. However, host high-affinity iron binding proteins limit levels of free iron in fluids and tissues. To overcome this deficiency of iron during infection, bacterial pathogens have developed iron uptake systems that are upregulated in the absence of iron, typically tightly controlled by the ferric uptake regulator (Fur) protein. The iron uptake system ofEdwardsiella ictaluri, a host-restricted pathogen of channel catfish (Ictalurus punctatus) and the main pathogen of this fish in aquaculture, is unknown. Here we describe theE. ictaluriFur protein, the iron uptake machinery controlled by Fur, and the effects offurgene deletion on virulence and immunogenicity in the fish host. Analysis of theE. ictaluriFur protein shows that it lacks the N-terminal region found in the majority of pathogen-encoded Fur proteins. However, it is fully functional in regulated genes encoding iron uptake proteins.E. ictalurigrown under iron-limited conditions upregulates an outer membrane protein (HemR) that shows heme-hemoglobin transport activity and is tightly regulated by Fur.In vivostudies showed that anE. ictaluriΔfurmutant is attenuated and immune protective in zebrafish (Danio rerio) and catfish (Ictalurus punctatus), triggering systemic immunity. We conclude that anE. ictaluriΔfurmutant could be an effective component of an immersion-oral vaccine for the catfish industry.

scholarly journals MgtE Homolog FicI Acts as a Secondary Ferrous Iron Importer inShewanella oneidensisStrain MR-1

2018 ◽  
Vol 84 (6) ◽  
Author(s):  
Brittany D. Bennett ◽  
Kaitlyn E. Redford ◽  
Jeffrey A. Gralnick
Keyword(s):  
Iron Uptake ◽  
Shewanella Oneidensis ◽  
Transport Proteins ◽  
Growth Defect ◽  
Wild Type ◽  
Content Type ◽  
Sequence Identity ◽  
Energy Dependent ◽  
Reducing Bacteria ◽  
Dependent Mechanism

ABSTRACTThe transport of metals into and out of cells is necessary for the maintenance of appropriate intracellular concentrations. Metals are needed for incorporation into metalloproteins but become toxic at higher concentrations. Many metal transport proteins have been discovered in bacteria, including the Mg2+transporter E (MgtE) family of passive Mg2+/Co2+cation-selective channels. Low sequence identity exists between members of the MgtE family, indicating that substrate specificity may differ among MgtE transporters. Under anoxic conditions, dissimilatory metal-reducing bacteria, such asShewanellaandGeobacterspecies, are exposed to high levels of soluble metals, including Fe2+and Mn2+. Here we characterize SO_3966, which encodes an MgtE homolog inShewanella oneidensisthat we name FicI (ferrousiron andcobaltimporter) based on its role in maintaining metal homeostasis. A SO_3966 deletion mutant exhibits enhanced growth over that of the wild type under conditions with high Fe2+or Co2+concentrations but exhibits wild-type Mg2+transport and retention phenotypes. Conversely, deletion offeoB, which encodes an energy-dependent Fe2+importer, causes a growth defect under conditions of low Fe2+concentrations but not high Fe2+concentrations. We propose that FicI represents a secondary, less energy-dependent mechanism for iron uptake byS. oneidensisunder high Fe2+concentrations.IMPORTANCEShewanella oneidensisMR-1 is a target of microbial engineering for potential uses in biotechnology and the bioremediation of heavy-metal-contaminated environments. A full understanding of the ways in whichS. oneidensisinteracts with metals, including the means by which it transports metal ions, is important for optimal genetic engineering of this and other organisms for biotechnology purposes such as biosorption. The MgtE family of metal importers has been described previously as Mg2+and Co2+transporters. This work broadens that designation with the discovery of an MgtE homolog inS. oneidensisthat imports Fe2+but not Mg2+. The research presented here also expands our knowledge of the means by which microorganisms have adapted to take up essential nutrients such as iron under various conditions.

Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells

Planta ◽  
2009 ◽  
Vol 229 (6) ◽  
pp. 1171-1179 ◽  
Author(s):  
Grégory Vert ◽  
Marie Barberon ◽  
Enric Zelazny ◽  
Mathilde Séguéla ◽  
Jean-François Briat ◽  
...  
Keyword(s):  
Iron Uptake ◽  
Iron Homeostasis ◽  
Epidermal Cells ◽  
Uptake System ◽  
High Affinity ◽  
Iron Uptake System

scholarly journals Impact of Na+-Translocating NADH:Quinone Oxidoreductase on Iron Uptake and nqrM Expression in Vibrio cholerae

2019 ◽  
Vol 202 (3) ◽  
Author(s):  
Shubhangi Agarwal ◽  
Melanie Bernt ◽  
Charlotte Toulouse ◽  
Hannes Kurz ◽  
Jens Pfannstiel ◽  
...  
Keyword(s):  
Vibrio Cholerae ◽  
Iron Uptake ◽  
Iron Homeostasis ◽  
Mrna Level ◽  
Strong Impact ◽  
Substrate Uptake ◽  
Uptake System ◽  
Content Type ◽  
Respiratory Enzyme ◽  
Nadh:Quinone Oxidoreductase

ABSTRACT The Na+ ion-translocating NADH:quinone oxidoreductase (NQR) from Vibrio cholerae is a membrane-bound respiratory enzyme which harbors flavins and Fe-S clusters as redox centers. The NQR is the main producer of the sodium motive force (SMF) and drives energy-dissipating processes such as flagellar rotation, substrate uptake, ATP synthesis, and cation-proton antiport. The NQR requires for its maturation, in addition to the six structural genes nqrABCDEF, a flavin attachment gene, apbE, and the nqrM gene, presumably encoding a Fe delivery protein. We here describe growth studies and quantitative real-time PCR for the V. cholerae O395N1 wild-type (wt) strain and its mutant Δnqr and ΔubiC strains, impaired in respiration. In a comparative proteome analysis, FeoB, the membrane subunit of the uptake system for Fe2+ (Feo), was increased in V. cholerae Δnqr. In this study, the upregulation was confirmed on the mRNA level and resulted in improved growth rates of V. cholerae Δnqr with Fe2+ as an iron source. We studied the expression of feoB on other respiratory enzyme deletion mutants such as the ΔubiC mutant to determine whether iron transport is specific to the absence of NQR resulting from impaired respiration. We show that the nqr operon comprises, in addition to the structural nqrABCDEF genes, the downstream apbE and nqrM genes on the same operon and demonstrate induction of the nqr operon by iron in V. cholerae wt. In contrast, expression of the nqrM gene in V. cholerae Δnqr is repressed by iron. The lack of functional NQR has a strong impact on iron homeostasis in V. cholerae and demonstrates that central respiratory metabolism is interwoven with iron uptake and regulation. IMPORTANCE Investigating strategies of iron acquisition, storage, and delivery in Vibrio cholerae is a prerequisite to understand how this pathogen thrives in hostile, iron-limited environments such as the human host. In addition to highlighting the maturation of the respiratory complex NQR, this study points out the influence of NQR on iron metabolism, thereby making it a potential drug target for antibiotics.

Evidence for a copper-dependent iron transport system in the marine, magnetotactic bacterium strain MV-1

Microbiology ◽  
2004 ◽  
Vol 150 (9) ◽  
pp. 2931-2945 ◽  
Author(s):  
Bradley L. Dubbels ◽  
Alan A. DiSpirito ◽  
John D. Morton ◽  
Jeremy D. Semrau ◽  
J. N. E. Neto ◽  
...  
Keyword(s):  
Iron Content ◽  
Iron Uptake ◽  
Iron Transport ◽  
Dna Analysis ◽  
Iron Concentration ◽  
Protein A ◽  
Uptake System ◽  
Iron Uptake System ◽  
Cellular Iron ◽  
Solid Media

Cells of the magnetotactic marine vibrio, strain MV-1, produce magnetite-containing magnetosomes when grown anaerobically or microaerobically. Stable, spontaneous, non-magnetotactic mutants were regularly observed when cells of MV-1 were cultured on solid media incubated under anaerobic or microaerobic conditions. Randomly amplified polymorphic DNA analysis showed that these mutants are not all genetically identical. Cellular iron content of one non-magnetotactic mutant strain, designated MV-1nm1, grown anaerobically, was ∼20- to 80-fold less than the iron content of wild-type (wt) MV-1 for the same iron concentrations, indicating that MV-1nm1 is deficient in some form of iron uptake. Comparative protein profiles of the two strains showed that MV-1nm1 did not produce several proteins produced by wt MV-1. To understand the potential roles of these proteins in iron transport better, one of these proteins was purified and characterized. This protein, a homodimer with an apparent subunit mass of about 19 kDa, was an iron-regulated, periplasmic protein (p19). Two potential ‘copper-handling’ motifs (MXM/MX2M) are present in the amino acid sequence of p19, and the native protein binds copper in a 1 : 1 ratio. The structural gene for p19, chpA (copper handling protein) and two other putative genes upstream of chpA were cloned and sequenced. These putative genes encode a protein similar to the iron permease, Ftr1, from the yeast Saccharomyces cerevisiae, and a ferredoxin-like protein of unknown function. A periplasmic, copper-containing, iron(II) oxidase was also purified from wt MV-1 and MV-1nm1. This enzyme, like p19, was regulated by media iron concentration and contained four copper atoms per molecule of enzyme. It is hypothesized that ChpA, the iron permease and the iron(II) oxidase might have analogous functions for the three components of the S. cerevisiae copper-dependent high-affinity iron uptake system (Ctr1, Ftr1 and Fet3, respectively), and that strain MV-1 may have a similar iron uptake system. However, iron(II) oxidase purified from both wt MV-1 and MV-1nm1 displayed comparable iron oxidase activities using O2 as the electron acceptor, indicating that ChpA does not supply the multi-copper iron(II) oxidase with copper.

scholarly journals Iron uptake system medicated by Vibrio anguillarum plasmid pJM1.

1983 ◽  
Vol 156 (2) ◽  
pp. 880-887 ◽  
Author(s):  
M A Walter ◽  
S A Potter ◽  
J H Crosa
Keyword(s):  
Iron Uptake ◽  
Vibrio Anguillarum ◽  
Uptake System ◽  
Iron Uptake System

scholarly journals Yeast protective response to arsenate involves the repression of the high affinity iron uptake system

2013 ◽  
Vol 1833 (5) ◽  
pp. 997-1005 ◽  
Author(s):  
Liliana Batista-Nascimento ◽  
Michel B. Toledano ◽  
Dennis J. Thiele ◽  
Claudina Rodrigues-Pousada
Keyword(s):  
Iron Uptake ◽  
Uptake System ◽  
Protective Response ◽  
High Affinity ◽  
Iron Uptake System

scholarly journals Dopamine Is a Siderophore-Like Iron Chelator That PromotesSalmonella entericaSerovar Typhimurium Virulence in Mice

mBio ◽  
2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Stefanie Dichtl ◽  
Egon Demetz ◽  
David Haschka ◽  
Piotr Tymoszuk ◽  
Verena Petzer ◽  
...  
Keyword(s):  
Bacterial Growth ◽  
Iron Uptake ◽  
Iron Homeostasis ◽  
Iron Acquisition ◽  
Lipocalin 2 ◽  
Intracellular Iron ◽  
Content Type ◽  
Hepcidin Expression

ABSTRACTWe have recently shown that the catecholamine dopamine regulates cellular iron homeostasis in macrophages. As iron is an essential nutrient for microbes, and intracellular iron availability affects the growth of intracellular bacteria, we studied whether dopamine administration impacts the course ofSalmonellainfections. Dopamine was found to promote the growth ofSalmonellaboth in culture and within bone marrow-derived macrophages, which was dependent on increased bacterial iron acquisition. Dopamine administration to mice infected withSalmonella entericaserovar Typhimurium resulted in significantly increased bacterial burdens in liver and spleen, as well as reduced survival. The promotion of bacterial growth by dopamine was independent of the siderophore-binding host peptide lipocalin-2. Rather, dopamine enhancement of iron uptake requires both the histidine sensor kinase QseC and bacterial iron transporters, in particular SitABCD, and may also involve the increased expression of bacterial iron uptake genes. Deletion or pharmacological blockade of QseC reduced but did not abolish the growth-promoting effects of dopamine. Dopamine also modulated systemic iron homeostasis by increasing hepcidin expression and depleting macrophages of the iron exporter ferroportin, which enhanced intracellular bacterial growth.Salmonellalacking all central iron uptake pathways failed to benefit from dopamine treatment. These observations are potentially relevant to critically ill patients, in whom the pharmacological administration of catecholamines to improve circulatory performance may exacerbate the course of infection with siderophilic bacteria.IMPORTANCEHere we show that dopamine increases bacterial iron incorporation and promotesSalmonellaTyphimurium growth bothin vitroandin vivo. These observations suggest the potential hazards of pharmacological catecholamine administration in patients with bacterial sepsis but also suggest that the inhibition of bacterial iron acquisition might provide a useful approach to antimicrobial therapy.

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