Iron acquisition pathways and colonization of the inflamed intestine by Salmonella enterica serovar Typhimurium

Highlights • Ferric iron uptake via IroN and TonB uptake contributes to fitness of Salmonella typhimurium in the inflamed intestine. • Ferrous iron uptake via FeoB contributes to Salmonella fitness in the intestine after antibiotic treatment. • The benefit conferred by FeoB after antibiotic treatmen...

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Published inInternational journal of medical microbiology Vol. 306; no. 8; pp. 604 - 610
Main Authors Costa, Luciana F, Mol, Juliana P.S, Silva, Ana Patricia C, Macêdo, Auricélio A, Silva, Teane M.A, Alves, Geraldo E.S, Winter, Sebastian, Winter, Maria G, Velazquez, Eric M, Byndloss, Mariana X, Bäumler, Andreas J, Tsolis, Renée M, Paixão, Tatiane A, Santos, Renato L
Format Journal Article
LanguageEnglish
Published Germany Elsevier GmbH 01.12.2016
Subjects
Animal models
Animals
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Cattle
Disease Models, Animal
Fe2
Fe3
Female
Gastroenteritis - microbiology
Infectious Disease
Inflammation
Intestines - microbiology
Iron - metabolism
Male
Medical Education
Metabolic Networks and Pathways - genetics
Mice, Inbred C57BL
Salmonella
Salmonella Infections - microbiology
Salmonella typhimurium - metabolism
Virulence Factors - genetics
Virulence Factors - metabolism
Fe 2
Salmonella
Animal models
Inflammation
Fe 3
Fe2
Fe3
Fe(2+)
Fe(3+)
Online AccessGet full text

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Abstract Highlights • Ferric iron uptake via IroN and TonB uptake contributes to fitness of Salmonella typhimurium in the inflamed intestine. • Ferrous iron uptake via FeoB contributes to Salmonella fitness in the intestine after antibiotic treatment. • The benefit conferred by FeoB after antibiotic treatment is independent of T3SS-induced intestinal inflammation. • Disruption of the gut microbiota by antibiotics may alter the availability of ferrous iron to colonizing Salmonella.
AbstractList •Ferric iron uptake via IroN and TonB uptake contributes to fitness of Salmonella typhimurium in the inflamed intestine.•Ferrous iron uptake via FeoB contributes to Salmonella fitness in the intestine after antibiotic treatment.•The benefit conferred by FeoB after antibiotic treatment is independent of T3SS-induced intestinal inflammation.•Disruption of the gut microbiota by antibiotics may alter the availability of ferrous iron to colonizing Salmonella. Salmonella enterica serotype Typhimurium is able to expand in the lumen of the inflamed intestine through mechanisms that have not been fully resolved. Here we utilized streptomycin-pretreated mice and dextran sodium sulfate (DSS)-treated mice to investigate how pathways for S. Typhimurium iron acquisition contribute to pathogen expansion in the inflamed intestine. Competitive infection with an iron uptake-proficient S. Typhimurium strain and mutant strains lacking tonB feoB, feoB, tonB or iroN in streptomycin pretreated mice demonstrated that ferric iron uptake requiring IroN and TonB conferred a fitness advantage during growth in the inflamed intestine. However, the fitness advantage conferred by ferrous iron uptake mechanisms was independent of inflammation and was only apparent in models where the normal microbiota composition had been disrupted by antibiotic treatment.
Salmonella enterica serotype Typhimurium is able to expand in the lumen of the inflamed intestine through mechanisms that have not been fully resolved. Here we utilized streptomycin-pretreated mice and dextran sodium sulfate (DSS)-treated mice to investigate how pathways for S. Typhimurium iron acquisition contribute to pathogen expansion in the inflamed intestine. Competitive infection with an iron uptake-proficient S. Typhimurium strain and mutant strains lacking tonB feoB, feoB, tonB or iroN in streptomycin pretreated mice demonstrated that ferric iron uptake requiring IroN and TonB conferred a fitness advantage during growth in the inflamed intestine. However, the fitness advantage conferred by ferrous iron uptake mechanisms was independent of inflammation and was only apparent in models where the normal microbiota composition had been disrupted by antibiotic treatment.
Salmonella enterica serotype Typhimurium is able to expand in the lumen of the inflamed intestine through mechanisms that have not been fully resolved. Here we utilized streptomycin-pretreated mice and dextran sodium sulfate (DSS)-treated mice to investigate how pathways for S. Typhimurium iron acquisition contribute to pathogen expansion in the inflamed intestine. Competitive infection with an iron uptake-proficient S. Typhimurium strain and mutant strains lacking tonB feoB, feoB, tonB or iroN in streptomycin pretreated mice demonstrated that ferric iron uptake requiring IroN and TonB conferred a fitness advantage during growth in the inflamed intestine. However, the fitness advantage conferred by ferrous iron uptake mechanisms was independent of inflammation and was only apparent in models where the normal microbiota composition had been disrupted by antibiotic treatment.
Highlights • Ferric iron uptake via IroN and TonB uptake contributes to fitness of Salmonella typhimurium in the inflamed intestine. • Ferrous iron uptake via FeoB contributes to Salmonella fitness in the intestine after antibiotic treatment. • The benefit conferred by FeoB after antibiotic treatment is independent of T3SS-induced intestinal inflammation. • Disruption of the gut microbiota by antibiotics may alter the availability of ferrous iron to colonizing Salmonella.
Author Byndloss, Mariana X
Paixão, Tatiane A
Alves, Geraldo E.S
Velazquez, Eric M
Macêdo, Auricélio A
Winter, Maria G
Tsolis, Renée M
Mol, Juliana P.S
Winter, Sebastian
Costa, Luciana F
Silva, Teane M.A
Santos, Renato L
Silva, Ana Patricia C
Bäumler, Andreas J
AuthorAffiliation 4 Department of Medical Microbiology and Immunology, University of California at Davis, Davis, CA, USA
3 Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, TX, USA
2 Departamento de Clínica e Cirurgia Veterinária, Escola de Veterinária da Universidade Federal Minas Gerais, Belo Horizonte, MG, Brazil
1 Departamento de Patologia, Instituto de Ciências Biológicas da Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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SSID ssj0002936
Score 2.3201365
Snippet Highlights • Ferric iron uptake via IroN and TonB uptake contributes to fitness of Salmonella typhimurium in the inflamed intestine. • Ferrous iron uptake via...
•Ferric iron uptake via IroN and TonB uptake contributes to fitness of Salmonella typhimurium in the inflamed intestine.•Ferrous iron uptake via FeoB...
Salmonella enterica serotype Typhimurium is able to expand in the lumen of the inflamed intestine through mechanisms that have not been fully resolved. Here we...
Salmonella enterica serotype Typhimurium is able to expand in the lumen of the inflamed intestine through mechanisms that have not been fully resolved. Here we...
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crossref
pubmed
elsevier
SourceType Open Access Repository
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Index Database
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StartPage 604
SubjectTerms Animal models
Animals
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Cattle
Disease Models, Animal
Fe2
Fe3
Female
Gastroenteritis - microbiology
Infectious Disease
Inflammation
Intestines - microbiology
Iron - metabolism
Male
Medical Education
Metabolic Networks and Pathways - genetics
Mice, Inbred C57BL
Salmonella
Salmonella Infections - microbiology
Salmonella typhimurium - metabolism
Virulence Factors - genetics
Virulence Factors - metabolism
Title Iron acquisition pathways and colonization of the inflamed intestine by Salmonella enterica serovar Typhimurium
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https://dx.doi.org/10.1016/j.ijmm.2016.10.004
https://www.ncbi.nlm.nih.gov/pubmed/27760693
https://www.proquest.com/docview/1835504484
https://pubmed.ncbi.nlm.nih.gov/PMC5140723
Volume 306
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