Low temperature (23 °C) increases expression of biofilm-, cold-shock- and RpoS-dependent genes in Escherichia coli K-12

Abstract

Temperature serves as a cue to regulate gene expression in Escherichia coli and other bacteria. Using DNA microarrays, we identified 297 genes whose expression is increased at 23 6C compared to 37 6C in E. coli K-12. Of these genes, 122 are RpoS-controlled, confirming genome-wide the model that low temperature serves as a primary cue to trigger the general stress response. Several genes expressed at 23 6C overlap with the cold-shock response, suggesting that strategies used to adapt to sudden shifts in temperature also mediate long-term growth at 23 6C. Another category of genes more highly expressed at 23 6C are associated with biofilm development, implicating temperature as an important cue influencing this developmental pathway. In a candidate set of genes tested, the biofilm genes (adrA, bolA, mlrA, nhaR, csgA, yceP/bssS) and cold-shock genes (otsA, yceP/bssS) were found to be RpoS-and DsrAdependent for their transcription at 23 6C. In contrast, transcription of three genes (ycgZ, dps and ymgB) was either partially or fully independent of these regulators, signifying there is an alternative thermoregulatory mechanism(s) that increases gene expression at 23 6C. Increased expression at 23 6C compared to 37 6C is retained in various media tested for most of the genes, supporting the relative importance of this cue in adaptation to changing environments. Both the RpoS-dependent gene otsA and the RpoS-independent gene ymgB demonstrated increased expression levels within 1 h after a shift from 37 to 23 6C, indicating a rapid response to this environmental cue. Despite changes in gene expression for many RpoS-dependent genes, experiments assessing growth rate at 23 6C and viability at 4 6C did not demonstrate significant impairment in rpoS : : Tn10 or dsrA : : cat mutant strains in comparison to the wild-type strain. Biofilm formation was favoured at low temperature and is moderately impaired in both the rpoS : : Tn10 and dsrA : : cat mutants at 23 6C, suggesting genes controlled by these regulators play a role necessary for optimal biofilm formation at 23 6C. Taken together, our data demonstrate that a large number of genes are increased in expression at 23 6C to globally respond to this environmental change and that at least two thermoregulatory pathways are involved in co-ordinating this response -the RpoS/DsrA pathway and an alternative thermoregulatory pathway, independent of these regulators.

Survey on Biofilm Production and Presence of Attachment Factors in Human Uropathogenic Strains of Escherichia coli

“…In fact, the biofilm synthesis regulation is highly complex, but little information is available on different species. Biofilm producing ability and correlation of different attachment factors were evaluated in several bacterial strains such as pathogenic Staphylococcus aureus (25) and E. coli (26)(27)(28).…”

Bacterial adaptation to cold

“…In a study focusing on E. coli biofilm formation at low temperatures, 40 % of the genes preferentially expressed at 23 u C were shown to be controlled by RpoS (White-Ziegler et al, 2008). Of these genes, several are implicated in biofilm development and an RpoS mutation decreases biofilm formation at 23 u C (White-Ziegler et al, 2008).…”

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

“…Consistent with this role, the Rcs phosphorelay has been shown to regulate the general stress response-associated sigma factor, s S , through the activation of RprA, a small non-coding RNA that positively controls the level of s S in the cell by base-pairing with the 59 end of the rpoS mRNA (Majdalani et al, 2001(Majdalani et al, , 2002. s S is involved in the adaptation of the bacteria to starvation, hyperosmotic shock, pH downshift and low temperature, and controls many genes during the transition from the exponential to the stationary phase of growth (Patten et al, 2004;Weber et al, 2005;White-Ziegler et al, 2008). Recent studies have reported that s S influences global gene expression and protein production within E. coli biofilms, suggesting that this alternative sigma factor may have an important function during biofilm formation (Collet et al, 2008;Ito et al, 2009).…”