FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions

Abstract

In Escherichia coli transcription of the tRNA operon thrU (tuJB) and the rRNA operon rrnB is trans-activated by the protein FIS. This protein, which stimulates the inversion of various viral DNA segments, binds specifically to a cis-acting sequence (designated UAS) upstream of the promoter of thrU (tuJB) and the P1 promoter of the rrnB operon. There are indications that this type of regulation is representative for the regulation of more stable RNA operons. In the present investigation we have studied UAS-dependent transcription activation of the thrU (tuiB) operon in the presence and absence of FIS during a normal bacterial growth cycle and after a nutritional shift-up. In early log phase the expression of the operon rises steeply in wild-type cells, whereafter it declines. Concomitantly, a peak of the cellular FIS concentration is observed.Cells in the stationary phase are depleted of FIS. The rather abrupt increase of transcription activation depends on the nutritional quality of the medium. It is not seen in minimal medium. After a shift from minimal to rich medium, a peak of transcription activation and of FIS concentration is measured. This peak gets higher as the medium gets more strongly enriched. We conclude that a correlation between changes of the UAS-dependent activation of the thrU (tuJB) operon and changes of the cellular FIS concentration under a variety of experimental conditions exists. This correlation strongly suggests that the production of FIS responds to environmental signals, thereby trans-activating the operon. Cells unable to produce FIS (fis cells) also show an increase of operon transcription in the early log phase and after a nutritional shift-up, albeit less pronounced than that of wild-type cells. Presumably it is controlled by the ribosome feedback regulatory system. cis activation of the operon by the upstream activator sequence is apparent in the absence of FIS. This activation is constant throughout the entire growth cycle and is independent of nutritional factors. The well-known growth rate-dependent control, displayed by exponentially growing cells studied under various nutritional conditions, is governed by two regulatory mechanisms: repression, presumably by ribosome feedback inhibition, and stimulation by trans activation. FIS allows very fast bacterial growth.The synthesis of rRNA of Escherichia coli is finely tuned to the cell's environmental conditions. Cells growing in a constant environment do not show a significant turnover or a significant buildup of free rRNA or vacant ribosomes, except at very low growth rates (for reviews, see references 20, 21, and 26). Consequently, ribosomes are utilized at maximal or near-maximal capacity. Upon alteration of the nutritional capacity of the medium, leading to a different but constant environment, cells promptly readjust the synthesis of their rRNA and tRNA to meet the demands of an altered growth rate. In exponentially growing cells the concentration of ribosomes (and of rRNA) thus appears to be proportional to growth rate (6,8...

DNA arms do the legwork to ensure the directionality of λ site-specific recombination

“…Excision is inhibited by high concentrations of IHF [19,20]. Because the cellular levels of IHF and Fis proteins respond to growth conditions, these host-encoded factors have been proposed as the master signals for integration and excision [15,[19][20][21][22][23].…”

The Escherichia coli fis Promoter Is Regulated by Changes in the Levels of Its Transcription Initiation Nucleotide CTP

“…In addition to mediating specialized site-specific DNA recombination events (1), this nucleoid-associated protein regulates transcription of ribosomal and tRNAs (2,3) and a growing number of structural genes (4 -16). Fis levels are transcriptionally regulated according to the nutritional conditions and the growth phase (17)(18)(19). A dramatic burst in fis mRNA levels is observed when stationary phase cells are outgrown in rich medium, which reach a peak during early logarithmic growth phase, decrease to much lower levels during late logarithmic growth phase, and become undetectable during stationary phase (17,18), an expression pattern that is closely followed at the protein level (17,19).…”

“…Fis levels are transcriptionally regulated according to the nutritional conditions and the growth phase (17)(18)(19). A dramatic burst in fis mRNA levels is observed when stationary phase cells are outgrown in rich medium, which reach a peak during early logarithmic growth phase, decrease to much lower levels during late logarithmic growth phase, and become undetectable during stationary phase (17,18), an expression pattern that is closely followed at the protein level (17,19). The fis mRNA half-life is short (about 2 min) and does not vary appreciably throughout the period of growth phase-dependent expression, indicating that the fis mRNA expression pattern is not attributed to changes in mRNA turnover rates but is primarily attributed to transcriptional control (20).…”

Fis regulates the competitiveness of Pseudomonas putida on barley roots by inducing biofilm formation

“…Global transcriptional factors can also be an important link between the environment and the physiological state of bacteria (Martínez-Antonio & Collado-Vides, 2003). For example, Fis (factor for inversion stimulation) triggers the fast growth of Escherichia coli in the presence of a sudden abundance of nutrients in the environment (Ball et al, 1992;Mallik et al, 2004;Nilsson et al, 1992). Bradley et al (2007) found that apart from the 231 genes that Fis regulates in E. coli, it activates the expression of a further 38 flagellar and motility genes as well.…”