Regulatory Role of PlaR (YiaJ) for Plant Utilization in Escherichia coli K-12

Abstract

Outside a warm-blooded animal host, the enterobacterium Escherichia coli K-12 is also able to grow and survive in stressful nature. The major organic substance in nature is plant, but the genetic system of E. coli how to utilize plant-derived materials as nutrients is poorly understood. Here we describe the set of regulatory targets for uncharacterized IclR-family transcription factor YiaJ on the E. coli genome, using gSELEX screening system. Among a total of 18 high-affinity binding targets of YiaJ, the major regulatory target was identified to be the yiaLMNOPQRS operon for utilization of ascorbate from fruits and galacturonate from plant pectin. The targets of YiaJ also include the genes involved in the utilization for other plant-derived materials as nutrients such as fructose, sorbitol, glycerol and fructoselysine. Detailed in vitro and in vivo analyses suggest that L-ascorbate and α-D-galacturonate are the effector ligands for regulation of YiaJ function. These findings altogether indicate that YiaJ plays a major regulatory role in expression of a set of the genes for the utilization of plant-derived materials as nutrients for survival. PlaR was also suggested to play protecting roles of E. coli under stressful environments in nature, including the formation of biofilm. We then propose renaming YiaJ to PlaR (regulator of plant utilization). Bacteria constantly monitor environmental conditions, and respond for adaptation and survival by modulating the expression pattern of their genomes. Transcription, the major regulation step in gene expression, is carried out by a single species of RNA polymerase (RNAP). The intracellular concentration of RNAP core enzyme in growing Escherichia coli K-12 W3110 strain is about 2,000 molecules per genome, which is less than the total of about 4,500 genes on its genome 1,2. The expression pattern of a total of about 4,500 genes in its genome, however, can be modulated through alteration of the promoter selectivity of RNAP after interaction with two groups of the regulatory proteins, i.e., seven species of the promoter recognition subunit sigma 1,3,4 and about 300 species of the DNA-binding transcription factors (TFs) 5,6. Based on the protein structure of DNA-binding motifs, these TFs were classified into 54 families (5; TEC database [www.shigen.nig.ac.jp/ecoli/tec/]). Up to the present time, more than 80% of the estimated 300 TFs in E. coli K-12 have been linked to at least one regulatory target gene or operon in its genome. The search for regulatory targets of these TFs has been carried out in vivo using both the ordinary molecular genetic approaches and the modern methodologies such as transcriptome using DNA microarrays and chromatin immunoprecipitation (ChIP) approaches. Using only in vivo analyses, however, it is difficult to get the complete set of regulatory targets because the binding in vivo of test TFs to their DNA targets is interfered with by both approximately 300 species of co-existing TFs and a number of nucleoid-associated DNA-binding proteins 5. The regulato...

Novel regulators of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli K-12

“…YhjC was renamed as RcdB (regulator B of the csgD promoter) while as to YiaJ, we recently identified its involvement in regulation of plant utilization (utilization of plant nutrients and colonization in plants) by E. coli and therefore renamed it as PlaR (regulator of plant utilization) [28]. The csgD promoter has been recognized as the most complex ‘multi-factor’ promoter in E.…”

“…Recently we found that YiaJ plays a regulatory role in expression of a set of the genes for the utilization of plant-derived materials as nutrients for survival outside host animals, and a group of the genes for colonization within plants under stressful environments in nature, including the formation of biofilm [28]. We then renamed YiaJ to PlaR (regulator of plant utilization).…”

“…Along this line, we propose to rename novel regulator YhjC as RcdB (regulator B of the csgD promoter). On the other hand, as with YiaJ, we recently identified its participation in regulation of a set of genes for utilizing plants (utilization of plant-derived compounds as nutrients and colonization in plants) and renamed it as PlaR (regulator of plant utilization) [28].…”

Microbial Musings – September 2020

“…They find that they can obtain strong evidence for two of these uncharacterized TFs, YiaJ (PlaR) and YhjC (RcdB), regulating the csgD promoter. For RcdB this is the first evidence for any promoter it regulates, while PlaR is a TF that they think from a related study is involved in regulating operons involved in the utilization of plant-derived nutrients, although this still needs further study [8]. The study reminds us that we still have plenty of biology to learn from this model organism, over 20 years after its genome was sequenced.…”

Expanded roles of pyruvate-sensing PdhR in transcription regulation of the Escherichia coli K-12 genome: fatty acid catabolism and cell motility

“…Table 1). A collection of 500-bp sequences from these targets was analysed using the dminda 2.0 program, which was successfully employed for the identification of the PlaR (regulator of plant utilization)-box sequence [13]. We identified a 17-bp-long sequence ( Fig.…”