Arch Microbiol (2010) 192:85–95 DOI 10.1007/s00203-009-0539-y

MI NI-R EVIE W

How do bacteria sense and respond to low temperature? S. Shivaji · Jogadhenu S. S. Prakash

Received: 24 September 2009 / Revised: 19 November 2009 / Accepted: 21 December 2009 / Published online: 5 January 2010 © Springer-Verlag 2010

Abstract RigidiWcation of the membrane appears to be the primary signal perceived by a bacterium when exposed to low temperature. The perception and transduction of the signal then occurs through a two-component signal transduction pathway consisting of a membrane-associated sensor and a cytoplasmic response regulator and as a consequence a set of cold-regulated genes are activated. In addition, changes in DNA topology due to change in temperature may also trigger cold-responsive mechanisms. Inducible proteins thus accumulated repair the damage caused by cold stress. For example, the Xuidity of the rigidiWed membrane is restored by altering the levels of saturated and unsaturated fatty acids, by altering the fatty acid chain length, by changing the proportion of cis to trans fatty acids and by changing the proportion of anteiso to iso fatty acids. Bacteria could also achieve membrane Xuidity changes by altering the protein content of the membrane and by altering the levels of the type of carotenoids synthesized. Changes in RNA secondary structure, changes in translation and alteration in protein conformation could also act as temperature sensors. This review highlights the various strategies by which bacteria senses

low temperature signal and as to how it responds to the change. Keywords Cold adaptation · Bacteria · Desaturases · Fatty acid synthesis · Two-component signal transduction pathway · DNA supercoiling Abbreviations Carbon regulation

Core enzyme ECF General stress response

GSP LPXTG motif Partner switching

RpoS

Communicated by Erko Stackebrandt.

Rsb SigB-GSR

S. Shivaji (&) Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500 007, India e-mail: [email protected]

SpeciWc stress/ starvation response

J. S. S. Prakash Department of Plant Sciences, School of Life Sciences, University of Hyderabad, Hyderabad, India

Vegetative dormancy

The preferred carbon source prevents the simultaneous utilization of alternative carbon sources Core enzyme of RNA polymerase (
2⬘-subunits) Extracytosolic function A stress response induced by a set of diverse environmental stimuli General stress proteins Amino acid motif for sortase anchoring Formation of alternative protein complexes that is controlled by protein phosphorylation Sigma factor of general stress response of E. coli and other Gram-negative bacteria Regulator of sigmaB SigB-dependent general stress response Induced by only one stimulus, adaptation against this stimulus only A quiescent metabolic state of vegetative cells

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Introduction The ability of microorganisms to adapt to low temperature conditions primarily depends on the ability of a sensor to sense changes in temperature. The membrane which acts as an interface between the external and internal environments of the cell could thus be one of the primary sensors of cold (Rowbury 2003). Therefore, survival at low temperature would depend on the ability of the sensor to perceive the signal and to transduce the signal to the genome ultimately bringing about up-regulation of genes whose products are likely to be involved in cold adaptation. These up-regulated genes could be categorized as follows: (1) genes for fatty acid desaturases (Sato and Murata 1980; Sato et al. 1979; Murata et al. 1992; Wada and Murata 1990); (2) genes that serve as RNA chaperones similar to the cold shock proteins (Csp) (Graumann et al. 1997; Hebraud and Potier 1999; Ermolenko and Makhatadze 2002; Goldstein et al. 1990); (3) genes involved in replication such as DnaA (replication initiation factor), RecA (DNA repair and maintenance protein), NusA (N-using substance A) and hns (DNA-binding global regulator) (Jones et al. 1987; Graumann and Marahiel 1999; Jones and Inouye 1994; Brandi et al. 1994); (4) genes involved in transcription such as rpoS (RNA polymerase sigma S) and sigD (RNA polymerase sigma factor D) (Kandror et al. 2002; Sledjeski et al. 1996; Majdalani et al. 1998; Inaba et al. 2003); (5) genes involved in translation such as fus (elongation factor), IF2 (translation initiation factor), IF2
(
form of translation initiation factor IF2), IF2 ( form of translation initiation factor IF2) and trmE (tRNA modiWcation GTPase) (Singh et al. 2009; Xia et al. 2003; Graumann and Marahiel 1999; Jones et al. 1987); (6) the hliA, hliB and hliC genes that encode high light-inducible proteins (Suzuki et al. 2001); (7) genes for a number of enzymes (Jones and Inouye 1994; Graumann and Marahiel 1999; Goodchild et al. 2004); and (8) various other genes that do not fall in any of the above categories (Prakash et al. 2009). A discussion on these genes and their products need to be dealt with separately in an independent review. The present review focuses on how bacteria sense low temperature and how they respond to the situation so as to survive the change.

Cold temperature sensing and signal transduction Model and biological membranes when exposed to cold temperatures exhibit reduction in lipid molecular dynamics due to a decrease in membrane Xuidity. This rigidiWcation of the membrane may be the cue to activate the sensor located in the membrane. In fact, this indeed may be so, because under isothermal conditions, reduction in the membrane Xuidity by palladium-catalyzed hydrogenation of the

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unsaturated fatty acids (Vigh et al. 1993) triggers one of the cold inducible genes, desA (codes for
12 acyl lipid desaturase), which in turn is under the control of a membrane-bound sensory kinase. Further, gene-engineered rigidiWcation of membrane was reported to enhance the inducibility of expression of cold-inducible genes (Inaba et al. 2003). These results suggest that decrease in membrane Xuidity serves as a primary signal for cold perception. Later, a two-component system consisting of a membranebound sensory kinase and a cytoplasmic response regulator was discovered to be involved in cold signal transduction (Suzuki et al. 2001; Los et al. 2008; Aguilar et al. 2001). The two-component signal transduction system is commonly referred to as the phosphor-transfer pathway since there is a transfer of a phosphate moiety from the sensor to the response regulator. The sensor is normally an integral membrane protein consisting of membrane-spanning domains, a signal-recognition domain and a kinase domain. Recognition of signal causes autophosphorylation of a histidine by the kinase, and the phosphate is then transferred to an aspartate on the response regulator which is present in the cytoplasm (Shivaji et al. 2007). However, in contrast to the above simple two-component signal transduction systems, multistep phosphorelay systems have been discovered in both prokaryotes and eukaryotes (Appleby et al. 1996; Zhang and Shi 2005). These multiple-step-type signal transduction pathways have a hybrid-type histidine kinase in which both the histidine kinase and the response regulator receiver domains are present in the same protein. Further, the histidine-containing phosphor-transfer domain could exist either as a domain in the hybrid-type histidine kinase or as a separate protein.

Sensors and transducers of low temperature in cyanobacteria In order to identify the low temperature sensor in cyanobacterial cells, Suzuki et al. (2000a) systematically inactivated each of the 43 putative histidine kinases genes (hik) in Synechocystis PCC 6803 and identiWed two histidine kinases namely a membrane-bound Hik33, a soluble Hik19 and a response regulator, Rer1 that aVected the inducibility of the desB gene(codes for
15 acyl lipid desaturase) (Suzuki et al. 2000a, b). Subsequently, it was demonstrated that the response regulator 26 (Rer26) along with Hik33 were involved in low temperature signal transduction (Suzuki et al. 2001; Mikami et al. 2002). Hik33 has a highly conserved histidine kinase domain at its carboxyl-terminus, two membrane-spanning domains at its amino terminus (Sakamoto and Murata 2002) and a type-P linker and a leucine zipper in the middle region characteristic of several membrane-bound histidine kinases from various organisms

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(Park et al. 1998). It was hypothesized that rigidiWcation of membrane lipids around Hik33 might alter the conformation of the membrane-spanning domains of Hik33 and as a consequence Hik33 would dimerize, become activated (Mikami et al. 2003; Taylor and Zhulin 1999; Suzuki et al. 2000a) and thus play the role of a global cold sensor (Inaba et al. 2003) (Fig. 1). In fact, studies proved beyond doubt that Hik33 recognizes a change in membrane Xuidity at low temperature (Szalontai et al. 2000). That hik33 is the sensor in Synechocystis PCC 6803 was further conWrmed by the observation that in mutants of hik33, half of the the coldinducible genes such as hliA, hliB and sigD, were no longer inducible by cold (Inaba et al. 2003). It was also observed that cold induction of some of the cold-inducible genes such as desA, desD (
6 acyl lipid desaturase) and crhL (ATP-dependent RNA helicase) was not aVected or only partially aVected as in the case of desB expression (Browse and Xin 2001; Suzuki et al. 2001) in mutants of hik33, thus indicating that a separate sensor apparently operates to regulate these genes. Further, Rer1, which functions downstream of Hik33 and Hik19, only regulates the cold induction of desB (
15 acyl lipid desaturase) and not of desA, desD or crhL, which presumably are regulated by additional response regulators or by a diVerent signaling mechanism.

Sensors and transducers of low temperature in Bacillus subtilis and Escherichia coli A membrane-associated two-component signal transduction pathway for cold signal perception consisting of DesK and DesR, the sensor and the response regulator, respectively, has also been identiWed in Bacillus subtilis (Kunst et al. 1997; Hoch 2000; Mansilla et al. 2003, 2005). DesK has four transmembrane segments that deWne the sensor domain and a long cytoplasmic C-terminal tail harboring the histidine kinase. This C-terminal kinase of DesK undergoes autophosphorylation in the presence of ATP and transfers a phosphate to DesR, the response regulator (Albanesi et al. 2004). Phosphorylated form of DesR, which is a transcriptional regulator, is directly involved in activation of the des genes at low temperatures (Aguilar et al. 2001; Cybulski et al. 2004). Thus, a regulatory loop consisting of DesK–DesR and unsaturated fatty acids constitute a novel mechanism for the sensing and transduction of low temperature signal in B. subtilis (Aguilar et al. 2001). Evidence that membrane Xuidity, rather than growth temperature, controls the transcription of the des gene was obtained by experiments in which the proportion of anteiso-branchedchain fatty acids of B. subtilis membranes was varied (Cybulski et al. 2002). Inactivation of desK or desR inhibited induction of des (Aguilar et al. 1999, 2001).

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Cold

Sa

S

P

R

P

Ra

?

hAMP PAS Kinase

? Gyrase

cold inducible genes

negatively super coiled DNA

Fig. 1 Diagrammatic representation of the two-component signal transduction pathway for the perception and transduction of low temperature signal in bacteria. The sensor (S) perceives the signal due to rigidiWcation of the membrane, gets activated by phosphorylation (Sa) and transfers the phosphate to the response regulator (R). The phosphorylated receptor (Ra) acts as a transcription regulator and brings about induction of cold-inducible genes whose products would help in cold adaptation. The model also demonstrates a link between expression of cold-inducible genes and DNA supercoiling. The organization of the sensor and the response regulator is shown separately. In Synechocystis PCC6803, the sensor has two transmembrane domains (shaded cylinders), the HAMP domain (histidine-kinase-adenylyl-cyclase-methyl-binding protein phosphatase), the PAS (PER-ARNFSIM) domain and the histidine kinase domain and the histidine residue (vertical rectangle with an H). The response regulator has a receiver domain with an aspartate residue (D), the transcriptional activation domain (ARNT) and the DNA-binding domain (HMG)

In Bacillus subtilis, DesK regulates DesR by acting either as a kinase or as a phosphatase, to phosphorylate or dephosphorylate DesR, in a temperature-dependent manner (Aguilar et al. 2001). At 37°C, DesK acts as a phosphatase and thus maintains DesR in an inactive dephosphorylated form. But following exposure to cold temperature, DesK phosphorylates DesR, which then binds to the des promotor region and up-regulates the expression of the gene (Aguilar et al. 1999; Beckering et al. 2002) ultimately leading to the synthesis of unsaturated fatty acids. The newly synthesized fatty acids would help to readjust the membrane Xuidity to the original level resulting in DesK, assuming the original conformation in which it existed prior to low temperature exposure. The similar CpxA-CpxR phosphorelay system, where CpxA is a histidine kinase containing transmembrane regions and the CpxR is a response regulator have also been investigated in Escherichia coli, Salmonella typhimurium and Yersinia pestis (de Wulf et al. 2000). In addition, in E. coli K-12, cold shock temporarily increases tumbling, whereas a temporary suppression of tumbling is observed after a sudden temperature upshift (Maeda et al. 1976; Nara et al. 1996). This phenomenon was observed only in chemotactically active strains of E. coli (W3110 and

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w3747), suggesting that the four classical methyl-accepting chemotaxis proteins (MCPs) Tsr, Tar, Trg and Tap represent a thermosensor in E. coli K-12 (Maeda and Imae 1979; Mizuno and Imae 1984; Nara et al. 1991). The exact mechanism of temperature-dependent alteration of the MCP-signaling state remains to be elucidated, but it is possible that temperature-dependent alterations of membrane Xuidity might cause the observed signaling states (Oosawa and Imae 1983, 1984).

Modulation of membrane Xuidity in bacteria in response to low temperature Survival of bacteria following low temperature exposure is dependent on the ability of the bacterium to restore its membrane Xuidity, which upon cold shock becomes rigid and impairs membrane-associated functions such as transport, energy generation and cell division. Therefore, in order to adapt to low temperature, it is crucial for the bacterium to be able to restore membrane function by increasing the Xuidity of the membrane. Bacteria modulate membrane Xuidity using various strategies such as by altering the size and charge of the polar head groups, by changing the proportion of short and long chain fatty acids, by changing the extent of fatty acid desaturation, by changing the proportion of cis and trans fatty acids and changing the composition of carotenoids (Kiran et al. 2004; Chattopadhyay et al. 1997). But studies have indicated that not all the above strategies are eVective. For instance, changes in the polar head groups are less frequent and less eVective in modifying the membrane Xuidity (Hasegawa et al. 1980; Suutari and Laakso 1994) and changes through chain length modiWcation is possible only in growing cells (Denich et al. 2003) and therefore may not be the universal method of modulating membrane Xuidity. Further, proteins by interacting with lipids contribute to the overall stability of the membrane bilayer (Epand 1998; Heipieper and de Bont 1994; Takeuchi et al. 1978, 1981), but the interaction itself is dependent on head group acylation, membrane Xuidity and membrane thickness, implying that it does not cause the primary eVect on Xuidity. Compared to the above strategies, changes in fatty acid desaturation, changes in fatty acid isomerisation and changes in composition of carotenoids appear to be the common modes of modulation of membrane Xuidity in cells growing or exposed to low temperatures.

Low temperature-dependent changes in fatty acid desaturation in bacteria Marr and Ingraham (1962) were the Wrst to demonstrate that E. coli responds to a decrease in temperature by

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increasing the amount of C18:1(11) and reducing palmitic acid C16:0 (Cronan and Gelmann 1973; Baldassare et al. 1976). It was also shown that FabF [3-oxoacyl-(acyl-carrier-protein) synthase II] that is required to convert C16:1(9) to C18:1(11) (Garwin et al. 1980) at low temperature in E. coli is independent of de novo synthesis of mRNA and protein (Garwin and Cronan 1980), thus implying that low temperature regulation of membrane Xuidity in E. coli is dependent on the activity of the enzyme and not the synthesis of FabF. All the above changes occur in the cytoplasmic membrane in response to cold adaptation but comparably little is known about the impact of low temperature on the outer membrane of Gram-negative bacteria. Lipopolysaccharide (LPS) is a major component of the outer leaXet of the outer membrane of Gram-negative bacteria and has three components: a polysaccharide that acts as an antigen, a hydrophobic membrane anchor known as lipid A and a core oligosaccharide that connects the antigen polymer to lipid A. The lipid A moiety of LPS is of interest since cold shock alters the de novo synthesis of the lipid A (Wollenweber et al. 1983; Carty et al. 1999) such that laurate is replaced by the unsaturated fatty acid palmitoleate in LPS (Carty et al. 1999) so as to readjust the outer membrane Xuidity after cold shock. A few years ago, Médigue et al. (2005) based on the genome sequence and in silico and in vivo analyses of an aqueous Antarctic psychrophilic bacterium Pseudoalteromonas haloplanktis (TAC125) discovered that this bacterium possesses unique features to adapt to the aqueous cold environment. It copes with the increased solubility of oxygen at low temperature by multiplying dioxygen-scavenging lipid desaturases while suppressing whole pathways producing reactive oxygen species. Dioxygen-consuming lipid desaturases achieve both protection against oxygen and synthesis of lipids making the membrane Xuid (Médigue et al. 2005). Bacillus subtilis and B. megaterium also convert already synthesized saturated fatty acids to unsaturated fatty acids when transferred to low temperature (Fulco 1969; Fujii and Fulco 1977; Diaz et al. 2002) by a desaturase coded by the des gene which is not detectable at 37°C but is induced transiently upon downshift in temperature (Aguilar et al. 1999). Membrane Xuidity is also increased in members of Bacillus by altering the levels of branched chain fatty acids since anteiso-branched-chain fatty acids increase the Xuidity of membranes compared to the corresponding isobranched-chain fatty acids (Kaneda 1991; Okuyama et al. 1991). Thus, it is apparent that Gram-positive bacteria like B. subtilis exhibit a dual strategy to restore membrane Xuidity after cold shock by increasing unsaturated fatty acids and anteiso fatty acids. Cyanobacteria have also been used as model systems to understand thermal regulation of membrane Xuidity. Most

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cyanobacteria respond to low temperature by increasing the level of the polyunsaturated fatty acid (C18:3(9,12,15)) at the expense of mono- and di-unsaturated fatty acids (C18:1(9) and C18:2(9,12)), respectively (Sato and Murata 1980; Sato et al. 1979; Murata et al. 1992; Wada and Murata 1990). These and other studies also demonstrated that polyunsaturated fatty acids and fatty acyl lipid desaturases are essential for the acclimation of cyanobacteria to low temperatures (Wada and Murata 1989; Murata and Wada 1995; Nishida and Murata 1996).

Low temperature-dependent changes in proportion of cis and trans fatty acids in bacteria Geometrical isomers such as the cis and trans fatty acids also aVect membrane Xuidity (Morita et al. 1993; Okuyama et al. 1990). Increased levels of cis-unsaturated fatty acids increase the Xuidity of the membrane since it provokes an unmovable kink of 30° in the acyl chain (Heipieper et al. 2003), whereas trans-unsaturated fatty acids decrease the Xuidity of the membrane. In Pseudomonas syringae (Lz4W), a psychrophilic bacterium from Antarctica, the proportion of saturated and trans-monounsaturated fatty acids increased when grown at 28°C compared to cells grown at 5°C, and the membrane Xuidity decreased with growth temperature (Kiran et al. 2004, 2005). Further, when the cti gene was mutated in P. syringae (Lz4W), it was observed that the growth of the mutant at 5°C was not altered but was arrested at 28°C, thus indicating that psychrophilic P. syringae requires trans-monounsaturated fatty acids for growth at higher temperatures (Kiran et al. 2004, 2005).

Low temperature-dependent changes in the composition of carotenoids in bacteria Growth temperature-dependent synthesis of a particular type of carotenoid (polar versus non-polar) may be a strategy to modulate membrane Xuidity since polar carotenoids stabilize the membrane to a greater extent than non-polar carotenoids (Jagannadham et al. 1991, 1996a, b, 2000; Chattopadhyay et al. 1997). In fact, in two psychrophilic bacteria, Sphingobacterium antarcticum (MTCC 675) and Micrococcus roseus (MTCC 678), the levels of polar carotenoids increased, whereas the levels of the less polar carotenoids decreased (Jagannadham et al. 2000; Chattopadhyay et al. 1997). Simultaneously, in S. antarcticum (MTCC 675), an increase in the biosynthesis of unsaturated and branched chain fatty acids in cells grown at 5°C compared to cells grown at 25°C was observed. Taken together, these results suggested that in cells grown at 5°C,

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the unsaturated and branched chain fatty acids, which increase quantitatively at low temperature, would increase the Xuidity of the membrane, whereas the polar carotenoids which stack well in the membrane would facilitate membrane stabilization and thus overcome the Xuidising eVect of the unsaturated fatty acids (Jagannadham et al. 1991, 1996a, 2000). This indeed could be a mechanism by which cells maintain homeoviscous adaptation, viz. an optimum membrane Xuidity. In fact, it was observed that the membrane Xuidity of intact cells of S. antarcticum (MTCC 675) was similar in cells grown at 5 and 25°C (Jagannadham et al. 2000). However, since psychrophilic bacteria synthesize higher amounts of polar carotenoids when grown at 5°C compared to 25°C, it is possible that these pigments modulate membrane Xuidity depending on the growth temperature.

Low temperature-induced accumulation of compatible solutes In response to various types of stress such as salt, cold, heat and free radicals, bacteria accumulate low molecular weight compounds (e.g., polyols, polyamines, sugars and amino acid derivatives) commonly referred to as compatible solutes. These compatible solutes protect cells from damage caused by stress by functioning as “chemical chaperones” and thus preventing denaturation and aggregation of proteins. Trehalose, glycine betaine and carnitine are a few of the compatible solutes that are known to accumulate following cold shock in bacteria (Kandror et al. 2002; Ko et al. 1994; Bayles and Wilkinson 2000; Becker et al. 2000). In E. coli, increase in trehalose is due to upregulation of otsAB operon (generates trehalose from glucose) when cells are shifted from 37 to 16°C (Kandror et al. 2002). The growth of otsA null mutants was not altered at 16°C, but viability of otsA null mutants is reduced when grown at 4°C. Thus, accumulation of trehalose may be an anticipatory defense mechanism to overcome stress at temperatures below 16°C. Analyses of the genome sequence of Colwellia psychrerythraea indicated that it produces polyhydroxyalkanoate compounds, which function as nitrogen reserves (Methe et al. 2005) and also produce compatible solutes, such as glycine betaine and extracellular polysaccharide compounds that can serve as cryoprotectants thus helping in cold adaptation (Methe et al. 2005). Rodrigues and Tiedje (2008) are of the opinion that bacteria adapt to extreme environments by networking of genes with some of them getting activated and others getting repressed, but the mechanism underlying this networking have not been explored in psychrophilic microorganisms. A good example here is the sigma B (alternative RNA polymerase sigma subunit) regulons in Bacillus, which involves hundreds of

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genes that overlap with other regulons, thus allowing a coordinated response to diverse stresses (Hecker et al. 2007).

Sensing low temperature through alteration in DNA conformation Eriksson et al. (2002) suggested that temperature-induced conformational or physico-chemical changes in DNA, RNA and proteins could form the basis for sensing temperature. The Wrst clue that DNA conformation may inXuence cold adaptation is based on the observation that the size and shape of B. subtilis does not change after cold shock, but low temperature exposure induces nucleoid compaction (Weber et al. 2001). This compaction may be due to one or more reasons such as (1) temperature-induced conformational change in DNA, (2) alteration in the activity and/or amounts of DNA proteins such as DNA gyrase (Jones et al. 1992), histone-like proteins including H-NS (La Teana et al. 1991; Dersch et al. 1994), HU (Wada et al. 1988; Giangrossi et al. 2002) and topoisomerase I and/or (3) impaired synthesis of proteins which inXuence condensation of the nucleoid (Woldringh et al. 1995). That DNA conformation is important for cold adaptation is also strengthened by the observation that in bacteria, the expression of many genes is dependent on DNA conformation, which in turn depends on temperature-dependent changes in DNA supercoiling (Grau et al. 1994; Hurme and Rhen 1998). In a recent paper, it has been demonstrated that inhibition of negative supercoiling leads to inhibition of cold-inducible gene expression, thus demonstrating a link between expression of cold-inducible genes and DNA supercoiling (Prakash et al. 2009) (Fig. 1). The topoisomerase II and I (Drlica 1992; Tse-Dinh et al. 1997) and the ‘nucleoid-associated’ proteins such as H-NS (Williams and Rimsky 1997; Dorman et al. 1999) regulate supercoiling. In Shigella, the expression of the virulence regulator, virF, at low temperature is suppressed by H-NS (Tobe et al. 1993), and the ability of H-NS to mediate transcriptional repression is dependent on the superhelical state of the promoter region (Falconi et al. 1998). However, when the temperature is increased to 37°C, the ability of H-NS to bind cooperatively to its target sequence at the virF promoter sequences decreases due to a conformational shift in the local DNA topology, allowing transcription of virF (Falconi et al. 1998). Furthermore, E. coli and many other bacteria express the protein StpA (Dorman et al. 1999; SonnenWeld et al. 2001), which also has a function similar to H-NS. Consequently, these proteins in concert with DNA appear to serve as an additional bacterial temperature perception system and may deWne a further cold-relevant regulatory element (Weber and Marahiel 2003).

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Sensing low temperature through alteration in RNA conformation RNA molecules due to their ability to form pronounced secondary and tertiary structures (Andersen and Delihas 1990) and their ability to form intermolecular RNA/RNA hybrids (Lease and Belfort 2000) have a strong potential to act as temperature sensors (Lai 2003; Narberhaus et al. 2005). Excellent examples are the protein LcrF, which in Yersinia pestis is a virulence regulator (Hoe and Gougen 1993; Straley and Perry 1995), and the virulence-activating transcription factor prfA from Listeria monocytogenes, which are thermoregulated (Romby and Ehresmann 2003). In these cases, the LcrF mRNA and prfA mRNA at 25°C are folded into a secondary structure, thus preventing translation (Hoe and Gougen 1993). However, at elevated temperature, the stem–loop structure melts, thus allowing translation. Thus, lcrF mRNA and prfA mRNA would serve as both the messenger and the thermosensor. In E. coli and Salmonella typhimurium, cold expression of RpoS is dependent on the expression of the dsrA gene encoding a small regulatory RNA (Sledjeski et al. 1996; Majdalani et al. 1998). The temperature-dependent expression of these small regulatory RNAs can modify the activity of proteins and the stability and translation of mRNAs and thus are critical to regulation of genes (Repoila and Gottesman 2003; Majdalani et al. 2005). Studies have demonstrated that the minimal dsrA promoter of 36 bp contains suYcient information to ensure temperature-dependent regulation, and the results favored an RNA polymerase-DNA interaction model instead of a trans-acting factor for temperature regulation (Repoila and Gottesman 2003).

Sensing low temperature through alteration in translation Cold shock is known to cause transient arrest in growth (Das and Goldstein 1968; Friedman et al. 1971; Broeze et al. 1978), and this may be attributed to a block in translation due to mRNAs containing more stable secondary structures at low temperature (15°C) compared to 37°C and as a consequence inhibit initiation and elongation of translation. But bacteria overcome this problem by RNA helicases that are cold induced (Jones et al. 1996; Chamot et al. 1999; Chamot and Owttrim 2000; Yu and Owttrim 2000), which remove RNA secondary structures and protect mRNA from RNase-mediated degradation (Lost and Dreyfus 1994). Studies have also indicated that following cold exposure, ribosomal proteins, translation factors and other components that help in the function and/or biogenesis of ribosomes are induced (Jones and Inouye 1996; Dammel and Noller 1995; Jones et al. 1996), thus implying that activation

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of the translation machinery is crucial for overcoming the deleterious eVects of cold temperature (Das and Goldstein 1968; Friedman et al. 1971; Broeze et al. 1978; Jones and Inouye 1996; Farewell and Neidhart 1998). These mechanisms have been observed both in E. coli and B. subtilis (Beckering et al. 2002; Kaan et al. 2002). A cold-induced ribosome-associated inhibitor protein, pY (RaiA), has been identiWed in E. coli. This protein pY stabilizes 70S ribosomes against dissociation (Agafonov et al. 1999) and inhibits translation by blocking the binding of aminoacyltRNA to the ribosomal A site (Agafonov et al. 2001). Therefore, it is not surprising that pY is present during low temperature-induced growth arrest in E. coli but disappears on growth resumption (Neuhaus et al. 2000).

Sensing low temperature through alteration in protein conformation Changes in protein conformation as a means for temperature sensing have been observed in bacteria. In Salmonella typhimurium TlpA, a 371-amino acid protein (Gulig et al. 1993; Hurme et al. 1996, 1997) has the capacity to sense temperature variations and to regulate gene expression. TlpA at 28°C has the capacity to oligomerise and bind DNA and suppress its own expression. But when temperature increases, the oligomerisation decreases, leading to a derepression of the target gene. The sensory capacity of TlpA is dependent on the coiled-coil structure of TlpA, which illustrates sensing of temperature through changes in protein conformation. Earlier studies had suggested that membrane proteins that undergo temperature-dependent phosphorylation– dephosphorylation in bacteria might act as sensors (Ray et al. 1994a, b). A correlation was observed between phosphorylation and dephosphorylation of a set of membrane proteins in response to upshift and downshift of temperature in the psychrophile P. syringae Lz4w (Ray et al. 1994a). In P. syringae Lz4W, it was also observed that the phosphorylated membrane protein could induce phosphorylation of a cystosolic 66-kDa protein (Ray et al. 1994b). In the same psychrophilic bacterium, diVerential phosphorylation of lipopolysaccharides was also observed in response to low temperature (Ray et al. 1994c).

Conclusions Membrane rigidiWcation appears to be the primary cue for low temperature sensing. This physical change in the packing of the fatty acids in the membranes is suYcient to activate a membrane-associated sensor. The sensor perceives and transduces the signal to a response regulator, which

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then induces up-regulation of genes involved in membrane Xuidity modulation. This two-component signal transduction system has been understood, to a limited extent, with respect to a few bacteria. Yet, we are far from understanding many key aspects of bacterial signal transduction in response to low temperature. For instance, there is a need to identify the sensor molecule(s) and the response regulators in various bacteria; a need to understand the cross talk between the above two components and ultimately the need to understand function of the response regulator as an inducer of gene expression. The domains in the sensor that perceive the change in membrane Xuidity and the lipid molecules that speciWcally interact with the sensor are yet not known. Therefore, studies directed toward Wnding answers to the above questions would ultimately unravel the molecular basis of low temperature perception, signal transduction and survival at low temperature. Acknowledgments This work was supported by a grant from the India–Japan Cooperative Science Programme of the Department of Science and Technology, Government of India and the Japanese Society for the Promotion of Science, Government of Japan and the Network Project titled “Exploitation of India’s rich microbial diversity” funded by CSIR to SS.

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