Journal of Bacteriology, January 2006, p. 587-598, Vol. 188, No. 2
0021-9193/06/$08.00+0 doi:10.1128/JB.188.2.587-598.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
YdgG (TqsA) Controls Biofilm Formation in Escherichia coli K-12 through Autoinducer 2 Transport
Moshe Herzberg,1
Ian K. Kaye,1
Wolfgang Peti,2 and
Thomas K. Wood1*
Departments of Chemical Engineering and Molecular & Cell Biology, University of Connecticut, 191 Auditorium Road, Storrs, Connecticut 06269-3222,1
Department of Molecular Pharmacology, Physiology, and Biotechnology, Brown University, 70 Ship Street GE3, Providence, Rhode Island 029122
Received 1 September 2005/
Accepted 27 October 2005
YdgG is an uncharacterized protein that is induced in Escherichia coli biofilms. Here it is shown that deletion of ydgG decreased extracellular and increased intracellular concentrations of autoinducer 2 (AI-2); hence, YdgG enhances transport of AI-2. Consistent with this hypothesis, deletion of ydgG resulted in a 7,000-fold increase in biofilm thickness and 574-fold increase in biomass in flow cells. Also consistent with the hypothesis, deletion of ydgG increased cell motility by increasing transcription of flagellar genes (genes induced by AI-2). By expressing ydgG in trans, the wild-type phenotypes for extracellular AI-2 activity, motility, and biofilm formation were restored. YdgG is also predicted to be a membrane-spanning protein that is conserved in many bacteria, and it influences resistance to several antimicrobials, including crystal violet and streptomycin (this phenotype could also be complemented). Deletion of ydgG also caused 31% of the bacterial chromosome to be differentially expressed in biofilms, as expected, since AI-2 controls hundreds of genes. YdgG was found to negatively modulate expression of flagellum- and motility-related genes, as well as other known products essential for biofilm formation, including operons for type 1 fimbriae, autotransporter protein Ag43, curli production, colanic acid production, and production of polysaccharide adhesin. Eighty genes not previously related to biofilm formation were also identified, including those that encode transport proteins (yihN and yihP), polysialic acid production (gutM and gutQ), CP4-57 prophage functions (yfjR and alpA), methionine biosynthesis (metR), biotin and thiamine biosynthesis (bioF and thiDFH), anaerobic metabolism (focB, hyfACDR, ttdA, and fumB), and proteins with unknown function (ybfG, yceO, yjhQ, and yjbE); 10 of these genes were verified through mutation to decrease biofilm formation by 40% or more (yfjR, bioF, yccW, yjbE, yceO, ttdA, fumB, yjiP, gutQ, and yihR). Hence, it appears YdgG controls the transport of the quorum-sensing signal AI-2, and so we suggest the gene name tqsA.
* Corresponding author. Mailing address: Departments of Chemical Engineering and Biology, Texas A & M University, 220 Jack E. Brown Building, College Station, TX 77843-3122. Phone: (979) 862-1588. Fax: (979) 845-6884. E-mail: Thomas.Wood{at}chemail.tamu.edu.
Journal of Bacteriology, January 2006, p. 587-598, Vol. 188, No. 2
0021-9193/06/$08.00+0 doi:10.1128/JB.188.2.587-598.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.
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Copyright © 2006 by the American Society for Microbiology. All rights reserved.