Systematic discovery of uncharacterized transcription factors in<i>Escherichia coli</i>K-12 MG1655

Gao, Ye; Yurkovich, James T.; Seo, Sang Woo; Kabimoldayev, Ilyas; Dräger, Andreas; Chen, Ke; Sastry, Anand V.; Fang, Xin; Mih, Nathan; Yang, Laurence T.; Eichner, Johannes; Cho, Byung-Kwan; Kim, Donghyuk; Palsson, Bernhard Ø.

doi:10.1101/343913

Cited by 12 publications

(32 citation statements)

References 69 publications

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“…Yet, except for ppGpp-controlled ribosome genes, the signals connecting the other genes subject to GRDC remain elusive. The regulatory roles of the 24 TFs genes shown in these two groups (Table 1) would be the first candidates to explore using a systematic method reported recently (Gao et al, 2018).…”

Section: Uncovering Gene Regulation Strategy At a Genomewide Scalementioning

confidence: 99%

Deciphering global gene expression and regulation strategy in Escherichia coli during carbon limitation

Pan

Xiao

et al. 2018

Microbial Biotechnology

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Summary Despite decades of studies meant to analyse the bacterial response to carbon limitation, we still miss a high‐resolution overview of the situation. All gene expression changes observed in such conditions cannot solely be accounted for by the global regulator Crp either free or bound to its effector, cyclic AMP . Here, for the first time, we evaluated the response of both CDS (protein‐coding sequence) and nc RNA (non‐coding RNA ) genes to carbon limitation, revealed cellular functions of differentially expressed genes systematically, quantified the contribution of Crp‐ cAMP and other factors to regulation and deciphered regulation strategies at a genomewide scale. Approximately one‐third of the differentially expressed genes we identified responded to Crp‐ cAMP via its direct or indirect control, while the remaining genes were subject to growth rate‐dependent control or were controlled by other regulators, especially RpoS. Importantly, gene regulation mechanisms can be established by expression pattern studies. Here, we propose a comprehensive picture of how cells respond to carbon scarcity. The global regulation strategies thus exposed illustrate that the response of cell to carbon scarcity is not limited to maintaining sufficient carbon metabolism via cAMP signalling while the main response is to adjust metabolism to cope with a slow growth rate.

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Section: Uncovering Gene Regulation Strategy At a Genomewide Scalementioning

confidence: 99%

Deciphering global gene expression and regulation strategy in Escherichia coli during carbon limitation

Pan

Xiao

et al. 2018

Microbial Biotechnology

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“…For the PRECISE experiments, the PhoB iModulon activity was significantly lower than the PhoB iModulon activity under the phosphate starvation condition in this study. For example, the experiment with the highest PhoB iModulon activity in PRECISE, a yddM knockout experiment (67), had a PhoB activity of 2.8, which is only 23% of the phosphate starvation condition PhoB iModulon activity of 11.8. The lower PhoB iModulon activities in the PRECISE experiments is consistent with the absence of phosphate starvation conditions in any of the previous experiments (Fig.…”

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confidence: 99%

Elucidation of regulatory modes for five two-component systems inEscherichia colireveals novel relationships

Choudhary¹,

Kleinmanns²,

Decker³

et al. 2020

Preprint

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23Escherichia coli uses two-component systems (TCSs) to respond to environmental 24 signals. TCSs affect gene expression and are parts of E. coli's global transcriptional regulatory 25 network (TRN). Here, we identified the regulons of five TCSs in E. coli MG1655: BaeSR and 26 CpxAR, which were stimulated by ethanol stress; KdpDE and PhoRB, induced by limiting 27 potassium and phosphate, respectively; and ZraSR, stimulated by zinc. We analyzed RNA-seq 28 data using independent component analysis (ICA). ChIP-exo data was used to validate condition-29 specific target gene binding sites. Based on this data we (1) identify the target genes for each 30 TCS; (2) show how the target genes are transcribed in response to stimulus; and (3) reveal novel 31 relationships between TCSs, which indicate non-cognate inducers for various response 32 regulators, such as BaeR to iron starvation, CpxR to phosphate limitation, and PhoB and ZraR to 33 cell envelope stress. Our understanding of the TRN in E. coli is thus notably expanded. 35Importance 36 E. coli is a common commensal microbe found in human gut microenvironment; 37 however, some strains cause diseases like diarrhea, urinary tract infections and meningitis. E. 38 coli's two-component system (TCS) modulates target gene expression, specially related to 39 virulence, pathogenesis and anti-microbial peptides, in response to environmental stimuli. Thus, 40 it is of utmost importance to understand the transcriptional regulation of the TCSs to infer its 41 environmental adaptation and disease pathogenicity. Utilizing a combinatorial approach 42 integrating RNAseq, independent component analysis, ChIP-exo and data mining, we show that 43 TCSs have five different modes of transcriptional regulation. Our data further highlights non-44 cognate inducers of TCSs emphasizing cross-regulatory nature of TCSs in E. coli and suggests 45 that TCSs may have a role beyond their cognate functionalities. In summary, these results when 46 further incorporated with genome scale metabolic models can lead to understanding of metabolic 47 capabilities of bacteria and correctly predict complex phenotype under diverse conditions. 48 49 Keywords 50 51 Two-component systems, E. coli, independent component analysis, transcriptomics, ChIP-exo, 52 transcriptional regulatory network, gene targets 53 54 Introduction 55 56Bacterial survival and resilience across diverse conditions relies upon environmental 57 sensing and a corresponding response. One pervasive biological design towards this goal consists 58 of a histidine kinase unit to sense the environment and a related response regulator unit to receive 59 the signal and translate it into gene expression changes. This signaling process is known as a 60 two-component system (TCS) (1). In the case of Escherichia coli (E. coli) strain K12 MG1655, 61 there are 30 histidine kinases and 32 response regulators involved in 29 complete two-62 component systems that mediate responses to various environmental stimuli such as metal 63 sen...

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“…After total RNA extraction, the quality was assessed using an Aglient Bioanalyser using an RNA 6000 kit after removal of ribosomal RNA. Paired-end strand specific RNA sequencing libraries were prepared as described (38).…”

Section: Methodsmentioning

confidence: 99%

“…RNA-and protein-free DNA samples were used to perform primer extension and second adaptor ligation with the following modifications. The DNA samples, incubated for primer extension as described previously (38) We constructed multiple alignments of the closely related species upstream regions for the genes that correspond to ChIP-exo protected areas. The length of the binding motif was limited to 15 bp using the MEME tool.…”

Section: Chip-exo Experimentsmentioning

confidence: 99%

PtrR (YneJ) is a novelE. colitranscription factor regulating the putrescine stress response and glutamate utilization

Rodionova

Gao

Sastry³

et al. 2020

Preprint

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Although polyamines, such as putrescine (Ptr), induce envelope stress for bacteria, they are important as nitrogen and carbon sources. Ptr utilization in Escherichia coli involves protein glutamylation, and glutamate stands at a crossroads between catabolism and anabolism. This communication reports that the transcription factor YneJ, here renamed PtrR, is involved in the regulation of a small regulatory RNA gene, fnrS, and an operon, yneIHGF, encoding succinatesemialdehyde dehydrogenase, Sad (YneI), glutaminase, GlsB (YneH), and several other genes.The yneI promoter is activated during putrescine utilization under nitrogen/carbon starvation conditions, and we show that PtrR is important for the putrescine stress response. It is also a repressor of fnrS gene expression, involved in the cascade regulation of mRNA synthesis for the marA and sodB genes, involved in antibiotic responses. PtrR transcriptional regulation of fnrS leads to a regulatory cascade induced by this small RNA that affects mRNA levels of ompF and the multidrug resistance regulator, MarA. We propose that PtrR functions as a dual activator/repressor, and that its regulation is important for the responses to different stress conditions involving L-glutamine/L-glutamate and putrescine utilization.

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Systematic discovery of uncharacterized transcription factors inEscherichia coliK-12 MG1655

Cited by 12 publications

References 69 publications

Deciphering global gene expression and regulation strategy in Escherichia coli during carbon limitation

Deciphering global gene expression and regulation strategy in Escherichia coli during carbon limitation

Elucidation of regulatory modes for five two-component systems inEscherichia colireveals novel relationships

PtrR (YneJ) is a novelE. colitranscription factor regulating the putrescine stress response and glutamate utilization

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