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Microbiology 154 (2008), 148-166; DOI  10.1099/mic.0.2007/012021-0
© 2008 Society for General Microbiology

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

Christine A. White-Ziegler, Suzin Um, Natalie M. Pérez, Abby L. Berns, Amy J. Malhowski and Sarah Young

Department of Biological Sciences and Program in Biochemistry, Smith College, Northampton, MA 01063, USA

Correspondence
Christine A. White-Ziegler
cwhitezi{at}smith.edu

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 °C compared to 37 °C 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 °C overlap with the cold-shock response, suggesting that strategies used to adapt to sudden shifts in temperature also mediate long-term growth at 23 °C. Another category of genes more highly expressed at 23 °C 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 DsrA-dependent for their transcription at 23 °C. 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 °C. Increased expression at 23 °C compared to 37 °C 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 °C, indicating a rapid response to this environmental cue. Despite changes in gene expression for many RpoS-dependent genes, experiments assessing growth rate at 23 °C and viability at 4 °C 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 °C, suggesting genes controlled by these regulators play a role necessary for optimal biofilm formation at 23 °C. Taken together, our data demonstrate that a large number of genes are increased in expression at 23 °C 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.


Abbreviations: COGs, clusters of orthologous groups of proteins; qRT-PCR, quantitative real-time RT-PCR

The GEO accession number for the microarray data reported in this paper is GSE9197.







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