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Review
. 2001 Jan 15;20(1-2):1-11.
doi: 10.1093/emboj/20.1.1.

The black cat/white cat principle of signal integration in bacterial promoters

I Cases  1 , V de Lorenzo
Affiliations
Review

The black cat/white cat principle of signal integration in bacterial promoters

I Cases et al. EMBO J. .
No abstract available

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Figures

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Fig. 1. Expression profiles and development of promoters responding to novel environmental signals (e.g. latest carbon sources). Expression of genes and gene clusters encoding new catabolic abilities towards an evolutionarily recent substrate may be simply achieved through constitutive expression (type 1). This may evolve further into inducible expression (type 2). The presence of other nutrients in the medium that are easier to metabolize can later influence such induction and cause a C-source inhibition (type 3). Finally, both the presence of other nutrients, growth rate, and other environmental and physiological signals can be integrated for downregulation of the promoter during rapid growth, causing the so-called exponential silencing (type 4).
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Fig. 2. Organization of the TOL and dmp biodegradation pathways and their cognate Pu and Po promoters. (A) The regulatory cascade of the xyl genes in the TOL plasmid pWW0 of P.putida mt-2. In the presence of upper pathway substrates like m-xylene, the upper-operon promoter Pu and the xylS promoter Ps are activated by XylR in combination with the σ54-containing RNA polymerase (σ54-RNAP). Subsequently, an excess of XylS product or XylS bound to its effectors (i.e. substrates of the meta pathway) activate Pm. There is no physical continuity between the upper and the meta operons. Below the scheme of the pathway, the Pu promoter region is expanded, showing the boundaries of relevant DNA sequences: upstream binding sites (UAS) for XylR, the –12/–24 sequences recognized by σ54-RNAP, and a single IHF binding site located within the intervening region. (B) Regulation of the pVI150-encoded dmp-operon of Pseudomonas sp. CF600. The dmpR gene product that is responsive to phenol and cresols activates transcription of the divergently transcribed dmp-operon from the Po promoter. A subset of the dmp genes are involved in phenol hydroxylation, while the rest encode enzymatic activities of the meta-cleavage pathway for dissimilation of the catechol intermediate. The Po promoter region is expanded below the scheme of the dmp pathway. Relevant portions of the sequence are pinpointed.
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Fig. 3. Integration of specific and physiological signals on the outcome of the Pu promoter of the TOL plasmid pWW0. This archetypal promoter receives both inducer-specific and overall physiological inputs. The specific regulation that makes Pu respond to toluene and xylenes involves only the XylR regulator. On the contrary, metabolic inputs are channeled towards the transcription machinery through multiple molecular assets. These include the control of the activity or the turnover of the σ54 factor in vivo (perhaps through the FtsH/DnaK system, or an antisigma factor or both) (Cases et al., 1996; Carmona and de Lorenzo, 1999), the action of the phosphorylated form of PtsN (Cases et al., 1999) and also the influence of intrinsic or factor (IHF)-mediated DNA bending. The related Po promoter of catabolic plasmid pVI150 (see Figure 2B) seems to react positively to the intracellular levels of the alarmone ppGpp (Sze et al., 1999), whereas the response of Pu to the stringent response is far less pronounced (Carmona et al., 2000).
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Fig. 4. Evolutionary optimization of promoter performance. The scheme illustrates the black cat/white cat principle discussed in the text. Promoters recruited to respond to novel enviromental signals, such as unfamiliar carbon sources, gravitate necessarily towards an optimal window of activity. Such a window is defined as the combination of: (i) the various working ranges of promoter gain/capacity (inducibility versus absolute promoter output); (ii) the specificity of the regulator/promoter pair for a given chemical; and (iii) the connection of promoter activity to the cell physiology. The drift towards such an optimal window is independent of the molecular mechanism to reach it. The presence of specific DNA/promoter/regulators combinations in front of given biodegradative operons thus reflect much more the evolutionary history of the system than a requirement for a distinct type of transcriptional factor.
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