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  • Review Article
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Promoters in the environment: transcriptional regulation in its natural context

Nature Reviews Microbiology volume 3, pages 105–118 (2005)Cite this article

Key Points

  • Transcriptional activation of most bacterial promoters in their natural environments is not a simple on/off decision, as the expression of cognate genes is integrated in layers of iterative regulatory networks that ensure the performance not only of the whole cell, but also of the bacterial population, and even of the entire microbial community, in a changing environment.

  • Promoters merge specific responses to distinct signals with reactions to more general environmental changes. The integration of multiple signals by distinct promoters in bacteria that inhabit complex niches is paramount for those interested in using microorganisms for the bioremediation of toxic chemicals.

  • The most well-studied example of environmental co-regulation of transcription has been the catabolic operons encoded by the TOL plasmid pWW0 of Pseudomonas putida, which control the degradation of toluene and m-xylene. One of the key components is the σ54-dependent promoter Pu, which responds to at least four different physiological/environmental inputs including m-xylene.

  • Although Pu is inhibited in vivo during rapid growth in rich medium, it can be transcribed in vitro by just combining purified IHF, σ54, core RNAP and the regulator. It is plausible that the mechanism (or mechanisms) that inhibit transcription in vivo, in response to multiple environmental signals, do so by preventing the binding of the σ54–RNAP to their target sites.

  • The extreme reductionist approaches of molecular biology have meant that it is now impractical to deal with large amounts of information on transcriptional control. One way forward is the application of network theory to regulation of gene expression. This approach allows ill-defined descriptions of complexity to be replaced by objectively quantifiable, numerical parameters, such as connectivity or density. The naive notion that 'everything is connected to everything' in biological systems is therefore quantified, categorized and properly understood.

  • While the global transcription network for individual cells is highly structured, several sub-networks appear more often than would be expected by mere chance. An intriguing possibility to account for this paradox is that evolutionary selection operates on the structure of the signal-integration and -regulatory networks, rather than on their individual components.

  • The genomes of bacteria that inhabit stable habitats (for instance, extremophiles, obligate symbionts and some intracellular pathogens) encode few regulators. By contrast, many other pathogens and free-living non-pathogenic organisms are more variable in their relative contents of transcriptional factors. A careful inspection of these groups revealed that the distinction in the share of regulators was related to the 'natural history' of each bacterium (that is, the life-style and degree of specialization).

Abstract

Transcriptional activation of many bacterial promoters in their natural environment is not a simple on/off decision. The expression of cognate genes is integrated in layers of iterative regulatory networks that ensure the performance not only of the whole cell, but also of the bacterial population, and even the microbial community, in a changing environment. Unlike in vitro systems, where transcription initiation can be recreated with a handful of essential components, in vivo, promoters must process various physicochemical and metabolic signals to determine their output. This helps to achieve optimal bacterial fitness in extremely competitive niches. Promoters therefore merge specific responses to distinct signals with inclusive reactions to more general environmental changes.

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Figure 1: Regulons and stimulons.
Figure 2: Downregulation of σ54 promoters in vivo reflects the binding of factors to target DNA sequences.
Figure 3: Regulation of n-alkane (octane) degradation by the alk system of the Pseudomonas putida GPo1 plasmid pOCT.
Figure 4: Features of transcription networks.

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Acknowledgements

We thank A. Valencia, C. Ouzounis, F. Rojo and V. Shingler for helpful discussions and apologize to investigators whose work was not cited because of space constraints. Work from our laboratories that has been cited in this article was funded by grants from the Spanish Ministry of Education and Science, the European Union and the Conservation Biology Programme of the Banco de Bilbao-Vizcaya Foundation.

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Authors and Affiliations

  1. Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas (CSIC), Campus de Cantoblanco, Madrid, 28049, Spain

    Ildefonso Cases & Víctor de Lorenzo

  2. Centro de Astrobiología, Instituto Nacional de Tecnica Aerospacial (INTA)-CSIC, Torrejón de Ardoz, 28850, Spain

    Víctor de Lorenzo

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  1. Ildefonso Cases
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Correspondence to Víctor de Lorenzo.

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DATABASES

Entrez

ArcA

crc

cyoB

FIS

FNR

FtsH

LRP

NahR

NarL

ptsN

Rsd

XylR

XylS

Glossary

REGULON

All the genes and gene clusters (operons) that respond to the same transcriptional regulator, which becomes competent for activation/repression of cognate promoters in response to a given environmental signal.

STIMULON

All the genes and gene clusters that are expressed in response to a distinct physicochemical input, regardless of the specific regulators that mediate such a response. Typically, one stimulon involves the action of more than one transcription factor.

CATABOLITE REPRESSION

Inhibition of the transport and/or metabolism of certain carbon sources when alternative and easier-to-consume nutrients are present in the medium. In practice, this leads to a preferential choice of one carbon source out of those available.

ENTNER–DOUDOROFF PATHWAY

One of the major metabolic routes for the consumption of carbohydrates in bacteria. Typically, glucose is phosphorylated to G6P, then converted into gluconolactone-P and eventually into 2-dehydro 3-deoxygluconate-P. This intermediate is then split into pyruvate and GA3P, which enter the rest of the glycolytic pathway at separate sites. Glucose can also be converted into gluconate, which can only be degraded through this pathway.

EXPONENTIAL SILENCING

The lack of activity of many promoters of biodegradative operons for recalcitrant carbon sources when cells grow exponentially in a rich medium.

ALARMONE

An intracellular signal molecule that is synthesized at high levels when cells face distinct types of environmental insults. The archetypical alarmone is (p)ppGpp, the production of which is triggered by, among other signals, amino-acid starvation.

STRINGENT RESPONSE

The traditional name given to all the transcriptional responses to elevated levels of intracellular ppGpp that are brought about by various nutritional and environmental stresses.

CONNECTIVITY

The number of connections that a particular node has in a network. The connectivity distribution reflects the frequency of nodes with each possible connectivity value in the network.

POWER-LAW DISTRIBUTION

The relationship between two scalar quantities x and y is such that the relationship can be written as y = axγ where a (the constant of proportionality) and γ (the exponent of the power law) are constants.

SCALE-FREE NETWORKS

Networks with the property that the number of links k that originate from a given node has a power-law distribution p(k)∼k−γ and therefore, a few network nodes (called hubs) become far more connected than the others. This distribution dramatically influences the way the network operates, as random failures are unlikely to harm an important hub, while damage targeted to highly connected nodes might make such networks collapse.

SMALL-WORLD

Small world networks are those in which most nodes are highly connected to their neighbours, that is, the nodes are highly clustered and have shorter paths between them.

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Cases, I., de Lorenzo, V. Promoters in the environment: transcriptional regulation in its natural context. Nat Rev Microbiol 3, 105–118 (2005). https://doi.org/10.1038/nrmicro1084

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