Few microorganisms are as versatile as Escherichia coli. An important member of the normal intestinal microflora of humans and other mammals, E. coli has also been widely exploited as a cloning host in recombinant DNA technology. But E. coli is more than just a laboratory workhorse or harmless intestinal inhabitant; it can also be a highly versatile, and frequently deadly, pathogen. Several different E. coli strains cause diverse intestinal and extraintestinal diseases by means of virulence factors that affect a wide range of cellular processes.

Pathogenic Escherichia coli

The study of microbial pathogenesis offers many unique research opportunities. The interaction between host and pathogen during disease is a dynamic battlefield where the microbe's clever strategies for survival and multiplication meet head on with the formidable defenses of the immune system. It is no wonder that the tactics employed by both participants in this struggle provide such interesting research topics for scientists of diverse disciplines. Major advances, fueled largely by the application of a genetic approach, have been made in the biochemistry, immunology, and cell biology of the host-parasite interaction. Among the many new insights is the recognition that bacterial pathogens have evolved highly sophisticated signal transduction systems controlling the coordinate expression of virulence determinants. In this minireview, I will discuss emerging themes that characterize these virulence regulatory systems and speculate on how these control strategies might contribute to the overall success of the microbe during pathogenesis. I refer the reader to several other full-length reviews and minireviews of areas related to microbial virulence and coordinate regulation (21, 24, 27, 28, 30, 52, 74). Because of

Environmental signals controlling expression of virulence determinants in bacteria.

The 70-kb virulence plasmid enables Yersinia spp. (Yersinia pestis, Y. pseudotuberculosis, and Y. enterocolitica) to survive and multiply in the lymphoid tissues of their host. It encodes the Yop virulon, an integrated system allowing extracellular bacteria to disarm the cells involved in the immune response, to disrupt their communications, or even to induce their apoptosis by the injection of bacterial effector proteins. This system consists of the Yop proteins and their dedicated type III secretion apparatus, called Ysc. The Ysc apparatus is composed of some 25 proteins including a secretin. Most of the Yops fall into two groups. Some of them are the intracellular effectors (YopE, YopH, YpkA/YopO, YopP/YopJ, YopM, and YopT), while the others (YopB, YopD, and LcrV) form the translocation apparatus that is deployed at the bacterial surface to deliver the effectors into the eukaryotic cells, across their plasma membrane. Yop secretion is triggered by contact with eukaryotic cells and controlled by proteins of the virulon including YopN, TyeA, and LcrG, which are thought to form a plug complex closing the bacterial secretion channel. The proper operation of the system also requires small individual chaperones, called the Syc proteins, in the bacterial cytosol. Transcription of the genes is controlled both by temperature and by the activity of the secretion apparatus. The virulence plasmid of Y. enterocolitica and Y. pseudotuberculosis also encodes the adhesin YadA. The virulence plasmid contains some evolutionary remnants including, in Y. enterocolitica, an operon encoding resistance to arsenic compounds.

The Virulence Plasmid of Yersinia, an Antihost Genome

Horizontal gene transfer plays a major role in microbial evolution. However, newly acquired sequences can decrease fitness unless integrated into preexisting regulatory networks. We found that the histone-like nucleoid structuring protein (H-NS) selectively silences horizontally acquired genes by targeting sequences with GC content lower than the resident genome. Mutations in hns are lethal in Salmonella unless accompanied by compensatory mutations in other regulatory loci. Thus, H-NS provides a previously unrecognized mechanism of bacterial defense against foreign DNA, enabling the acquisition of DNA from exogenous sources while avoiding detrimental consequences from unregulated expression of newly acquired genes. Characteristic GC/AT ratios of bacterial genomes may facilitate discrimination between a cell's own DNA and foreign DNA.

https://science.sciencemag.org/content/sci/313/5784/236.full.pdf

Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella.

Like many eukaryotes, bacteria make widespread use of postreplicative DNA methylation for the epigenetic control of DNA-protein interactions. Unlike eukaryotes, however, bacteria use DNA adenine methylation (rather than DNA cytosine methylation) as an epigenetic signal. DNA adenine methylation plays roles in the virulence of diverse pathogens of humans and livestock animals, including pathogenic Escherichia coli, Salmonella, Vibrio, Yersinia, Haemophilus, and Brucella. In Alphaproteobacteria, methylation of adenine at GANTC sites by the CcrM methylase regulates the cell cycle and couples gene transcription to DNA replication. In Gammaproteobacteria, adenine methylation at GATC sites by the Dam methylase provides signals for DNA replication, chromosome segregation, mismatch repair, packaging of bacteriophage genomes, transposase activity, and regulation of gene expression. Transcriptional repression by Dam methylation appears to be more common than transcriptional activation. Certain promoters are active only during the hemimethylation interval that follows DNA replication; repression is restored when the newly synthesized DNA strand is methylated. In the E. coli genome, however, methylation of specific GATC sites can be blocked by cognate DNA binding proteins. Blockage of GATC methylation beyond cell division permits transmission of DNA methylation patterns to daughter cells and can give rise to distinct epigenetic states, each propagated by a positive feedback loop. Switching between alternative DNA methylation patterns can split clonal bacterial populations into epigenetic lineages in a manner reminiscent of eukaryotic cell differentiation. Inheritance of self-propagating DNA methylation patterns governs phase variation in the E. coli pap operon, the agn43 gene, and other loci encoding virulence-related cell surface functions.

Epigenetic Gene Regulation in the Bacterial World

Expression of specific adhesive properties by bacteria in general seems to be regulated to fit the environmental conditions. An example is the transcriptional regulation of digalactoside-specific binding by uropathogenic strains of Escherichia coli. The fimbrial structures (pili) on the bacterial surface carry the adhesin and are present during growth at 37 degrees C but are not produced by cells at lower temperatures, such as 25 degrees C. Thermoregulation of expression is due to temperature-dependent transcription of a regulatory cistron in the pilus-adhesin gene cluster. We have now identified and characterized a new regulatory locus (drdX) and show that a histone-like bacterial protein has an important role in this novel example of thermoregulation of transcription.

Transcriptional silencing and thermoregulation of gene expression in Escherichia coli

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Transcriptional silencing and thermoregulation of gene expression in Escherichia coli