The Highly Conserved Escherichia coli Transcription Factor YhaJ Regulates Aromatic Compound Degradation

Palevsky, Noa; Shemer, Benjamin; Connolly, James P. R.; Belkin, Shimshon

doi:10.3389/fmicb.2016.01490

Cited by 22 publications

(24 citation statements)

References 25 publications

(36 reference statements)

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“…Daley et al (28), based on bioinformatics data, postulated that this gene encodes a transmembrane quinol oxidase subunit, which could explain the strong response of the yqjF-based reporter toward quinol and its derivatives, including THT. This is supported by recent findings regarding the regulatory protein YhaJ, which regulates the expression of yqjF and several other genes, all related to the biotransformation of quinol-like compounds (29). While this may suggest a possible role of YqjF in the downstream transformation of THT, a deletion of yqjF did not result in any significant effect on the yqjF::lux reporter's response toward DNT (our unpublished data).…”

Section: Discussionsupporting

confidence: 86%

Aerobic Transformation of 2,4-Dinitrotoluene by Escherichia coli and Its Implications for the Detection of Trace Explosives

Shemer

Yagur‐Kroll

Hazan

et al. 2018

Appl Environ Microbiol

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DNT (2,4-dinitrotoluene), a volatile impurity in military-grade 2,4,6-trinitrotoluene (TNT)-based explosives, is a potential tracer for the detection of buried landmines and other explosive devices. We have previously described an bioreporter strain engineered to detect traces of DNT and have demonstrated that the gene promoter, the sensing element of this bioreporter, is induced not by DNT but by at least one of its transformation products. In the present study, we have characterized the initial stages of DNT biotransformation in , have identified the key metabolic products in this reductive pathway, and demonstrate that the main DNT metabolite that induces is 2,4,5-trihydroxytoluene. We further show that cannot utilize DNT as a sole carbon or nitrogen source and propose that this compound is metabolized in order to neutralize its toxicity to the cells. The information provided in this article sheds new light both on the microbial biodegradability of nitroaromatic compounds and on the metabolic capabilities of By doing so, it also clarifies the pathway leading to the previously unexplained induction of the gene by 2,4-dinitrotoluene, an impurity that accompanies 2,4,6-trinitrotoluene (TNT)-based explosives. Our improved understanding of these processes will serve to molecularly enhance the performance of a previously described microbial bioreporter of buried landmines and other explosive devices, in which the gene promoter serves as the sensing element.

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Section: Discussionsupporting

confidence: 86%

Aerobic Transformation of 2,4-Dinitrotoluene by Escherichia coli and Its Implications for the Detection of Trace Explosives

Shemer

Yagur‐Kroll

Hazan

et al. 2018

Appl Environ Microbiol

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“…S6). These data correlate well with the RNA-seq analysis in identifying directly regulated targets such as several virulence factors, the GAD acid tolerance response, and the known target yqjF (24).…”

Section: Resultssupporting

confidence: 72%

“…1 B ). Most significantly, the down-regulation of virulence coincided with the up-regulation of several genes of the GAD acid fitness network ( P = 6.16 × 10 −7 ) and differential expression of the known YhaJ target gene yqjF (24).…”

Section: Resultsmentioning

confidence: 97%

“…These targets included known regulated genes ( ybiJ , yoaC , yqjF , yhaK , and yhhW ) but also targets found both on the core E. coli genome (13 targets including the GAD regulator gene gadX ) as well as 5 EHEC-specific sequences ( SI Appendix , Fig. S4) (24, 26). Strikingly, these EHEC targets were located within cryptic prophage regions and upstream of genes encoding the pathotype-specific virulence factor nleA ( P = 8.5 × 10 −4 ) and 2 identical autotransporters, Z1211 and Z1651 , identified previously as Ag43 homologs Cah1 and Cah2 (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Distinct intraspecies virulence mechanisms regulated by a conserved transcription factor

Connolly

O’Boyle

Turner

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Tailoring transcriptional regulation to coordinate the expression of virulence factors in tandem with the core genome is a hallmark of bacterial pathogen evolution. Bacteria encode hundreds of transcription factors forming the base-level control of gene regulation. Moreover, highly homologous regulators are assumed to control conserved genes between members within a species that harbor the same genetic targets. We have explored this concept in 2 Escherichia coli pathotypes that employ distinct virulence mechanisms that facilitate specification of a different niche within the host. Strikingly, we found that the transcription factor YhaJ actively regulated unique gene sets between intestinal enterohemorrhagic E. coli (EHEC) and extraintestinal uropathogenic E. coli (UPEC), despite being very highly conserved. In EHEC, YhaJ directly activates expression of type 3 secretion system components and effectors. Alternatively, YhaJ enhances UPEC virulence regulation by binding directly to the phase-variable type 1 fimbria promoter, driving its expression. Additionally, YhaJ was found to override the universal GAD acid tolerance system but exclusively in EHEC, thereby indirectly enhancing type 3 secretion pleiotropically. These results have revealed that within a species, conserved regulators are actively repurposed in a “personalized” manner to benefit particular lifestyles and drive virulence via multiple distinct mechanisms.

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“…To confirm this phenomenon, we analyzed a known YhaJ target gene, yqjF, and similarly found that occupancy was not conditionally dependent or driven by YhaJ expression (see Fig. S1 in the supplemental material) (18). These results collectively indicate that differences in YhaJ enrichment at conserved sites are not exclusively driven by unexpected variations in TF dosage between members of the same species.…”

mentioning

confidence: 70%

Widespread Strain-Specific Distinctions in Chromosomal Binding Dynamics of a Highly Conserved Escherichia coli Transcription Factor

Connolly

O’Boyle

Roe

2020

mBio

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Bacterial gene regulation is governed by often hundreds of transcription factors (TFs) that bind directly to targets on the chromosome. Global studies of TFs usually make assumptions that regulatory targets within model strains will be conserved between members of the same species harboring common genetic targets. We recently discovered that YhaJ of Escherichia coli is crucial for virulence in two different pathotypes but binds to distinct regions of their genomes and regulates no common genes. This surprising result leads to strain-specific mechanisms of virulence regulation, but the implications for other E. coli pathotypes or commensals were unclear. Here, we report that heterogenous binding of YhaJ is widespread within the E. coli species. We analyzed the global YhaJ binding dynamics of four evolutionarily distinct E. coli isolates under two conditions, revealing 78 significant sites on the core genome as well as horizontally acquired loci. Condition-dependent dosage of YhaJ correlated with the number of occupied sites in vivo but did not significantly alter its enrichment at regions bound in both conditions, explaining the availability of this TF to occupy accessory sites in response to the environment. Strikingly, only ∼15% of YhaJ binding sites were common to all strains. Furthermore, differences in enrichment of uncommon sites were observed largely in chromosomal regions found in all strains and not explained exclusively by binding to strain-specific horizontally acquired elements or mutations in the DNA binding sequence. This observation suggests that intraspecies distinctions in TF binding dynamics are a widespread phenomenon and represent strain-specific gene regulatory potential. IMPORTANCE In bacterial cells, hundreds of transcription factors coordinate gene regulation and thus are a major driver of cellular processes. However, the immense diversity in bacterial genome structure and content makes deciphering regulatory networks challenging. This is particularly apparent for the model organism Escherichia coli as evolution has driven the emergence of species members with highly distinct genomes, which occupy extremely different niches in nature. While it is well-known that transcription factors must integrate horizontally acquired DNA into the regulatory network of the cell, the extent of regulatory diversity beyond single model strains is unclear. We have explored this concept in four evolutionarily distinct E. coli strains and show that a highly conserved transcription factor displays unprecedented diversity in chromosomal binding sites. Importantly, this diversity is not restricted to strain-specific DNA or mutation in binding sites. This observation suggests that strain-specific regulatory networks are potentially widespread within individual bacterial species.

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The Highly Conserved Escherichia coli Transcription Factor YhaJ Regulates Aromatic Compound Degradation

Cited by 22 publications

References 25 publications

Aerobic Transformation of 2,4-Dinitrotoluene by Escherichia coli and Its Implications for the Detection of Trace Explosives

Aerobic Transformation of 2,4-Dinitrotoluene by Escherichia coli and Its Implications for the Detection of Trace Explosives

Distinct intraspecies virulence mechanisms regulated by a conserved transcription factor

Widespread Strain-Specific Distinctions in Chromosomal Binding Dynamics of a Highly Conserved Escherichia coli Transcription Factor

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