Global impact of mature biofilm lifestyle on Escherichia coli K‐12 gene expression

Abstract

SummaryThe formation of biofilm results in a major lifestyle switch that is thought to affect the expression of multiple genes and operons. We used DNA arrays to study the global effect of biofilm formation on gene expression in mature Escherichia coli K-12 biofilm. We show that, when biofilm is compared with the exponential growth phase, 1.9% of the genes showed a consistent up-or downregulation by a factor greater than two, and that 10% of the E. coli genome is significantly differentially expressed. The functions of the genes induced in these conditions correspond to stress response as well as energy production, envelope biogenesis and unknown functions. We provide evidence that the expression of stress envelope response genes, such as the psp operon or elements of the cpx and rpoE pathways, is a general feature of E. coli mature biofilms. We also compared biofilm with the stationary growth phase and showed that the biofilm lifestyle, although sharing similarities with the stationary growth phase, triggers the expression of specific sets of genes. Using gene disruption of 54 of the most biofilm-induced genes followed by a detailed phenotypic study, we validated the biological relevance of our analysis and showed that 20 of these genes are required for the formation of mature biofilm. This group includes 11 genes of previously unknown function. These results constitute a comprehensive analysis of the global transcriptional response triggered in mature E. coli biofilms and provide insights into its physiological signature.

Escherichia coli transcription factor YncC (McbR) regulates colanic acid and biofilm formation by repressing expression of periplasmic protein YbiM (McbA)

“…Among the most induced genes, ptsH (4.0-fold) encodes a heat-stable histidyl phosphorylatable protein (Postma et al, 1993) that is induced by BssR/BssS in biofilms (Domka et al, 2006). Also induced was cpxP (4.6-fold) that encodes a periplasmic adaptor protein involved in resistance to extracytoplasmic stress (Danese and Silhavy, 1998), which was induced in E. coli TG1 and TG biofilms (Beloin et al, 2004) and is involved in adhesion of E. coli (Otto and Silhavy, 2002). sixA was induced 4.0-fold and encodes a signal inhibitory factor-X (Ogino et al, 1998) that was induced in E. coli TG1 and TG biofilms (Beloin et al, 2004).…”

“…Also induced was cpxP (4.6-fold) that encodes a periplasmic adaptor protein involved in resistance to extracytoplasmic stress (Danese and Silhavy, 1998), which was induced in E. coli TG1 and TG biofilms (Beloin et al, 2004) and is involved in adhesion of E. coli (Otto and Silhavy, 2002). sixA was induced 4.0-fold and encodes a signal inhibitory factor-X (Ogino et al, 1998) that was induced in E. coli TG1 and TG biofilms (Beloin et al, 2004). fldA was induced 5.3-fold and encodes flavodoxin 1 (Puan et al, 2005) that was induced in the human urine biofilms of the asymptomatic E. coli bacteriuria strains (Hancock and Klemm, 2007).…”

“…Hundreds of genes are differentially expressed during this biofilm development process (Schembri et al, 2003;Beloin et al, 2004;Ren et al, 2004a) and bacterial signaling such as quorum and metabolite sensing and catabolite repression are involved in this process (Jackson et al, 2002;Stanley and Lazazzera, 2004;Camilli and Bassler, 2006).…”

Modelling the spatial dynamics of plasmid transfer and persistence

“…Thus, the corresponding rates found in mass-action models are not a priori appropriate for use in IPS models for plasmid-bacteria dynamics on surfaces, and we must estimate these rates for our model based on spatial empirical data. Another reason for scepticism in applying parameter estimates from liquid experiments to surface populations is the fact that surface-attached bacteria can be physiologically quite different from their planktonic counterparts (Beloin et al, 2004).…”

Elevated levels of σ S inhibit biofilm formation in Escherichia coli: a role for the Rcs phosphorelay

“…Genetic studies suggest that gene expression during biofilm formation is temporally regulated and, as a consequence, cells will have different expression profiles at different times during the biofilm formation process (Beloin et al, 2004;Domka et al, 2007;Sauer et al, 2002). In particular, a variety of cell-surface appendages, including flagella and pili, are required for the initial attachment to the surface, whilst the transition to a mature biofilm involves the production of an exopolysaccharide-rich matrix by the bacteria (Danese et al, 2000a, b;O'Toole & Kolter, 1998;Pratt & Kolter, 1998;Prigent-Combaret et al, 2000).…”