Iron induces bimodal population development by Escherichia coli.
Bacterial biofilm formation is a complex developmental process involving cellular differentiation and the formation of intricate 3D structures. Here we demonstrate that exposure to ferric chloride triggers rugose biofilm formation by the uropathogenic Escherichia coli strain UTI89 and by enteric bacteria Citrobacter koseri and Salmonella enterica serovar typhimurium. Two unique and separable cellular populations emerge in iron-triggered, rugose biofilms. Bacteria at the air-biofilm interface express high levels of the biofilm regulator csgD, the cellulose activator adrA, and the curli subunit operon csgBAC. Bacteria in the interior of rugose biofilms express low levels of csgD and undetectable levels of matrix components curli and cellulose. Iron activation of rugose biofilms is linked to oxidative stress. Superoxide generation, either through addition of phenazine methosulfate or by deletion of sodA and sodB, stimulates rugose biofilm formation in the absence of high iron. Additionally, overexpression of Mn-superoxide dismutase, which can mitigate iron-derived reactive oxygen stress, decreases biofilm formation in a WT strain upon iron exposure. Not only does reactive oxygen stress promote rugose biofilm formation, but bacteria in the rugose biofilms display increased resistance to H(2)O(2) toxicity. Altogether, we demonstrate that iron and superoxide stress trigger rugose biofilm formation in UTI89. Rugose biofilm development involves the elaboration of two distinct bacterial populations and increased resistance to oxidative stress.
Department of Microbiology and Immunology, University of Michigan, Ann Arbor, MI 48109, USA.
William H
WH
DePas
David A
DA
Hufnagel
John S
JS
Lee
Luz P
LP
Blanco
Hans C
HC
Bernstein
Steve T
ST
Fisher
Garth A
GA
James
Philip S
PS
Stewart
Matthew R
MR
Chapman
D018441:Biofilms / Q000187:drug effects / Q000254:growth & development*; D015153:Blotting, Western; D002712:Chlorides / Q000494:pharmacology*; D041041:Citrobacter koseri / Q000187:drug effects / Q000254:growth & development*; D054308:Enteropathogenic Escherichia coli / Q000187:drug effects / Q000254:growth & development*; D029968:Escherichia coli Proteins / Q000378:metabolism; D005290:Ferric Compounds / Q000494:pharmacology*; D006861:Hydrogen Peroxide / Q000378:metabolism; D018613:Microscopy, Confocal; D010100:Oxygen / Q000378:metabolism; D017382:Reactive Oxygen Species / Q000378:metabolism; D012486:Salmonella typhimurium / Q000187:drug effects / Q000254:growth & development*; D013482:Superoxide Dismutase / Q000378:metabolism; D015534:Trans-Activators / Q000378:metabolism; D001616:beta-Galactosidase / Q000378:metabolism
D002712:Chlorides; C499694:CsgD protein, E coli; D029968:Escherichia coli Proteins; D005290:Ferric Compounds; D017382:Reactive Oxygen Species; D015534:Trans-Activators; D006861:Hydrogen Peroxide; D013482:Superoxide Dismutase; D001616:beta-Galactosidase; D010100:Oxygen; C024555:ferric chloride