Transcriptional Regulation in Bacteria

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Molecular Microbiology and Immunology".

Deadline for manuscript submissions: closed (30 September 2024) | Viewed by 13425

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Guest Editor
School of Agriculture, Meiji University, Kawasaki, Japan
Interests: transcription factor; transcriptional regulation; genomic SELEX; RNA polymerase; sigma factor; Escherichia coli; genome regulation
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Special Issue Information

Dear Colleagues,

The goal of research in the post-genomic era, now that the full extent of the genes encoded by microbial genomes is known, is to elucidate the whole mechanism by which microorganisms utilize genes through transcriptional regulation. Deciphering the genome sequence of microorganisms has revealed its gene set and the set of transcriptional regulators that regulate those genes, providing a complete overview of transcriptional regulation in microorganisms. The number of target genes depends on the function of the transcription factor; some single-target regulators target a single gene in the genome, while others are global regulators that target hundreds of genes. In some cases, these have been shown to cooperate or antagonize each other at hundreds or more sites on the genome, dynamically regulating gene transcription.

It has also become clear that transcription factors comprehensively regulate multiple genes involved in multiple seemingly unrelated biological functions. Thus, analyses of transcriptional regulation reveal not only the molecular mechanisms of transcriptional regulation, but also the functional network of genes, leading to the elucidation of new physiological mechanisms of microorganisms.

This Special Issue aims to collect recent studies on microorganisms, from detailed and precise studies on the transcriptional regulatory mechanisms of single genes, to studies on the genome regulatory networks of whole genes, to newly revealed microorganism mechanisms.

Dr. Tomohiro Shimada
Guest Editor

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Keywords

  • transcription
  • gene regulation
  • genome regulation
  • regulatory network
  • RNA polymerase
  • sigma factor
  • transcription factor
  • nucleoid

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Published Papers (10 papers)

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Research

24 pages, 4095 KiB  
Article
It Takes Two to Make a Thing Go Right: Epistasis, Two-Component Response Systems, and Bacterial Adaptation
by Brittany R. Sanders, Lauren S. Thomas, Naya M. Lewis, Zaria A. Ferguson, Joseph L. Graves, Jr. and Misty D. Thomas
Microorganisms 2024, 12(10), 2000; https://doi.org/10.3390/microorganisms12102000 - 30 Sep 2024
Viewed by 707
Abstract
Understanding the interplay between genotype and fitness is a core question in evolutionary biology. Here, we address this challenge in the context of microbial adaptation to environmental stressors. This study explores the role of epistasis in bacterial adaptation by examining genetic and phenotypic [...] Read more.
Understanding the interplay between genotype and fitness is a core question in evolutionary biology. Here, we address this challenge in the context of microbial adaptation to environmental stressors. This study explores the role of epistasis in bacterial adaptation by examining genetic and phenotypic changes in silver-adapted Escherichia coli populations, focusing on the role of beneficial mutations in two-component response systems (TCRS). To do this, we measured 24-hour growth assays and conducted whole-genome DNA and RNA sequencing on E. coli mutants that confer resistance to ionic silver. We showed recently that the R15L cusS mutation is central to silver resistance, primarily through upregulation of the cus efflux system. However, here we show that this mutation’s effectiveness is significantly enhanced by epistatic interactions with additional mutations in regulatory genes such as ompR, rho, and fur. These interactions reconfigure global stress response networks, resulting in robust and varied resistance strategies across different populations. This study underscores the critical role of epistasis in bacterial adaptation, illustrating how interactions between multiple mutations and how genetic backgrounds shape the resistance phenotypes of E. coli populations. This work also allowed for refinement of our model describing the role TCRS genes play in bacterial adaptation by now emphasizing that adaptation to environmental stressors is a complex, context-dependent process, driven by the dynamic interplay between genetic and environmental factors. These findings have broader implications for understanding microbial evolution and developing strategies to combat antimicrobial resistance. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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17 pages, 3272 KiB  
Article
AraC Functional Suppressors of Mutations in the C-Terminal Domain of the RpoA Subunit of the Escherichia coli RNA Polymerase
by Dominique Belin, Jordan Costafrolaz and Filo Silva
Microorganisms 2024, 12(9), 1928; https://doi.org/10.3390/microorganisms12091928 - 23 Sep 2024
Viewed by 555
Abstract
In E. coli, transcriptional activation is often mediated by the C-terminal domain of RpoA, the α subunit of RNA polymerase. Random mutations that prevent activation of the arabinose PBAD promoter are clustered in the RpoA C-terminal domain (α-CTD). We have isolated [...] Read more.
In E. coli, transcriptional activation is often mediated by the C-terminal domain of RpoA, the α subunit of RNA polymerase. Random mutations that prevent activation of the arabinose PBAD promoter are clustered in the RpoA C-terminal domain (α-CTD). We have isolated functional suppressors of rpoA α-CTD mutations that map to araC, the main transcriptional regulator of ara genes, or to the PBAD promoter. No mutation was found in the DNA regulatory region between araC and PBAD. Most suppressors that improve PBAD transcription are localized to the N-terminal domain of AraC. One class of araC mutations generates substitutions in the core of the N-terminal domain, suggesting that they affect its conformation. Other suppressors localize to the flexible N-terminal arm of AraC. Some, but not all, suppressors confer an arabinose constitutive phenotype. Suppression by both classes of araC mutations requires the α-CTD to stimulate expression from PBAD. Surprisingly, in rpoA+ strains lacking Crp, the cAMP receptor protein, these araC mutations largely restore arabinose gene expression and can essentially bypass Crp activation. Thus, the N-terminal domain of AraC exhibits at least three distinct activities: dimerization, arabinose binding, and transcriptional activation. Finally, one mutation maps to the AraC C-terminal domain and can synergize with AraC mutations in the N-terminal domain. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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12 pages, 6006 KiB  
Article
HigA2 (Rv2021c) Is a Transcriptional Regulator with Multiple Regulatory Targets in Mycobacterium tuberculosis
by Mingyan Xu, Meikun Liu, Tong Liu, Xuemei Pan, Qi Ren, Tiesheng Han and Lixia Gou
Microorganisms 2024, 12(6), 1244; https://doi.org/10.3390/microorganisms12061244 - 20 Jun 2024
Viewed by 1036
Abstract
Toxin-antitoxin (TA) systems are the major mechanism for persister formation in Mycobacterium tuberculosis (Mtb). Previous studies found that HigBA2 (Rv2022c-Rv2021c), a predicted type II TA system of Mtb, could be activated for transcription in response to multiple stresses such as [...] Read more.
Toxin-antitoxin (TA) systems are the major mechanism for persister formation in Mycobacterium tuberculosis (Mtb). Previous studies found that HigBA2 (Rv2022c-Rv2021c), a predicted type II TA system of Mtb, could be activated for transcription in response to multiple stresses such as anti-tuberculosis drugs, nutrient starvation, endure hypoxia, acidic pH, etc. In this study, we determined the binding site of HigA2 (Rv2021c), which is located in the coding region of the upstream gene higB2 (Rv2022c), and the conserved recognition motif of HigA2 was characterized via oligonucleotide mutation. Eight binding sites of HigA2 were further found in the Mtb genome according to the conserved motif. RT-PCR showed that HigA2 can regulate the transcription level of all eight of these genes and three adjacent downstream genes. DNA pull-down experiments showed that twelve functional regulators sense external regulatory signals and may regulate the transcription of the HigBA2 system. Of these, Rv0903c, Rv0744c, Rv0474, Rv3124, Rv2603c, and Rv3583c may be involved in the regulation of external stress signals. In general, we identified the downstream target genes and possible upstream regulatory genes of HigA2, which paved the way for the illustration of the persistence establishment mechanism in Mtb. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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22 pages, 5205 KiB  
Article
Sigma Factor Engineering in Actinoplanes sp. SE50/110: Expression of the Alternative Sigma Factor Gene ACSP50_0507 (σHAs) Enhances Acarbose Yield and Alters Cell Morphology
by Laura Schlüter, Tobias Busche, Laila Bondzio, Andreas Hütten, Karsten Niehaus, Susanne Schneiker-Bekel, Alfred Pühler and Jörn Kalinowski
Microorganisms 2024, 12(6), 1241; https://doi.org/10.3390/microorganisms12061241 - 20 Jun 2024
Viewed by 1197
Abstract
Sigma factors are transcriptional regulators that are part of complex regulatory networks for major cellular processes, as well as for growth phase-dependent regulation and stress response. Actinoplanes sp. SE50/110 is the natural producer of acarbose, an α-glucosidase inhibitor that is used in diabetes [...] Read more.
Sigma factors are transcriptional regulators that are part of complex regulatory networks for major cellular processes, as well as for growth phase-dependent regulation and stress response. Actinoplanes sp. SE50/110 is the natural producer of acarbose, an α-glucosidase inhibitor that is used in diabetes type 2 treatment. Acarbose biosynthesis is dependent on growth, making sigma factor engineering a promising tool for metabolic engineering. ACSP50_0507 is a homolog of the developmental and osmotic-stress-regulating Streptomyces coelicolor σHSc. Therefore, the protein encoded by ACSP50_0507 was named σHAs. Here, an Actinoplanes sp. SE50/110 expression strain for the alternative sigma factor gene ACSP50_0507 (sigHAs) achieved a two-fold increased acarbose yield with acarbose production extending into the stationary growth phase. Transcriptome sequencing revealed upregulation of acarbose biosynthesis genes during growth and at the late stationary growth phase. Genes that are transcriptionally activated by σHAs frequently code for secreted or membrane-associated proteins. This is also mirrored by the severely affected cell morphology, with hyperbranching, deformed and compartmentalized hyphae. The dehydrated cell morphology and upregulation of further genes point to a putative involvement in osmotic stress response, similar to its S. coelicolor homolog. The DNA-binding motif of σHAs was determined based on transcriptome sequencing data and shows high motif similarity to that of its homolog. The motif was confirmed by in vitro binding of recombinantly expressed σHAs to the upstream sequence of a strongly upregulated gene. Autoregulation of σHAs was observed, and binding to its own gene promoter region was also confirmed. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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17 pages, 6279 KiB  
Article
A Comparative Transcriptome Analysis Unveils the Mechanisms of Response in Feather Degradation by Pseudomonas aeruginosa Gxun-7
by Chaodong Song, Rui Liu, Doudou Yin, Chenjie Xie, Ying Liang, Dengfeng Yang, Mingguo Jiang, Hongyan Zhang and Naikun Shen
Microorganisms 2024, 12(4), 841; https://doi.org/10.3390/microorganisms12040841 - 22 Apr 2024
Viewed by 1396
Abstract
Microbial degradation of feathers offers potential for bioremediation, yet the microbial response mechanisms warrant additional investigation. In prior work, Pseudomonas aeruginosa Gxun-7, which demonstrated robust degradation of feathers at elevated concentrations, was isolated. However, the molecular mechanism of this degradation remains only partially [...] Read more.
Microbial degradation of feathers offers potential for bioremediation, yet the microbial response mechanisms warrant additional investigation. In prior work, Pseudomonas aeruginosa Gxun-7, which demonstrated robust degradation of feathers at elevated concentrations, was isolated. However, the molecular mechanism of this degradation remains only partially understood. To investigate this, we used RNA sequencing (RNA-seq) to examine the genes that were expressed differentially in P. aeruginosa Gxun-7 when exposed to 25 g/L of feather substrate. The RNA-seq analysis identified 5571 differentially expressed genes; of these, 795 were upregulated and 603 were downregulated. Upregulated genes primarily participated in proteolysis, amino acid, and pyruvate metabolism. Genes encoding proteases, as well as those involved in sulfur metabolism, phenazine synthesis, and type VI secretion systems, were notably elevated, highlighting their crucial function in feather decomposition. Integration of Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) taxonomies, combined with a review of the literature, led us to propose that metabolic feather degradation involves environmental activation, reducing agent secretion, protease release, peptide/amino acid uptake, and metabolic processes. Sulfite has emerged as a critical activator of keratinase catalysis, while cysteine serves as a regulatory mediator. qRT–PCR assay results for 11 selected gene subset corroborated the RNA-seq findings. This study enhances our understanding of the transcriptomic responses of P. aeruginosa Gxun-7 to feather degradation and offers insights into potential degradation mechanisms, thereby aiding in the formulation of effective feather waste management strategies in poultry farming. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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12 pages, 3783 KiB  
Article
A Novel Regulator PepR Regulates the Expression of Dipeptidase Gene pepV in Bacillus thuringiensis
by Xin Zhang, Hengjie Wang, Tinglu Yan, Yuhan Chen, Qi Peng and Fuping Song
Microorganisms 2024, 12(3), 579; https://doi.org/10.3390/microorganisms12030579 - 14 Mar 2024
Cited by 1 | Viewed by 1253
Abstract
Bacillus thuringiensis produces insecticidal crystal proteins encoded by cry or cyt genes and targets a variety of insect pests. We previously found that a strong promoter of a DeoR family transcriptional regulator (HD73_5014) can efficiently drive cry1Ac expression in B. thuringiensis HD73. Here, [...] Read more.
Bacillus thuringiensis produces insecticidal crystal proteins encoded by cry or cyt genes and targets a variety of insect pests. We previously found that a strong promoter of a DeoR family transcriptional regulator (HD73_5014) can efficiently drive cry1Ac expression in B. thuringiensis HD73. Here, we investigated the regulation of neighbor genes by HD73_5014. The HD73_5014 homologs are widely distributed in Gram-positive bacterial species. Its neighbor genes include pepV, rsuA, and ytgP, which encode dipeptidase, rRNA pseudouridine synthase and polysaccharide biosynthesis protein, respectively. The four open reading frames (ORFs) are organized to be a pepR gene cluster in HD73. RT-PCR analysis revealed that the rsuA and ytgP genes formed a transcriptional unit (rsuA-ytgP operon), while pepV formed a transcriptional unit in HD73. Promoter-lacZ fusion assays showed that the pepV and rsuA-ytgP promoters are regulated by HD73_5014. EMSA experiments showed that HD73_5014 directly binds to the pepV promoter region but not to the rusA-ytgP promoter region. Thus, the HD73_5014 transcriptional regulator, which controls the expression of the dipeptidase pepV, was named PepR (dipeptidase regulator). We also confirmed the direct regulation between PepR and PepV by the increased sensitivity to vancomycin in ΔpepV and ΔpepR mutants compared to HD73. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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11 pages, 1812 KiB  
Article
The LiaSR Two-Component System Regulates Resistance to Chlorhexidine in Streptococcus mutans
by Shan Huang, Jing Huang, Jingyun Du, Yijun Li, Minjing Wu, Shuai Chen, Ling Zhan and Xiaojing Huang
Microorganisms 2024, 12(3), 468; https://doi.org/10.3390/microorganisms12030468 - 26 Feb 2024
Viewed by 1289
Abstract
Chlorhexidine (CHX) is widely considered to be the gold standard for preventing dental caries. However, it is possible to induce resistance to CHX. The LiaSR two-component system has been identified that contributed to CHX resistance in Streptococcus mutans, which is one of [...] Read more.
Chlorhexidine (CHX) is widely considered to be the gold standard for preventing dental caries. However, it is possible to induce resistance to CHX. The LiaSR two-component system has been identified that contributed to CHX resistance in Streptococcus mutans, which is one of the major pathogens in dental caries. However, the underlying mechanisms remain unclear. In this study, an MIC assay and a viability assessment demonstrated that after deleting the liaS and liaR genes, the sensitivity of mutants could increase. The Nile Red efflux assay exhibited that the efflux rates of mutants were significantly decreased. The RT-qPCR results indicated that the LiaSR two-component system-mediating influence on the expression of lmrB in S. mutans contributed to the efflux rate. The hydrophobicity assay and membrane potential assay showed that the mutants had higher levels of hydrophobicity and depolarization, suggesting that their membranes were more easily disturbed. The TEM graphs revealed that the border of the cell membrane was unclear in mutants compared with the wild-type strain, indicating that the cell envelope’s stress response may have been inhibited. While the surface charge of mutants showed no significant difference in the wild-type strain according to the result of cytochrome c-based charged determination. This study provides valuable novel insights into the mechanisms of the LiaSR two-component system in the CHX resistance of S. mutans. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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16 pages, 1743 KiB  
Article
Gene Expression of Ethanol and Acetate Metabolic Pathways in the Acinetobacter baumannii EmaSR Regulon
by Yu-Weng Huang, Hung-Yu Shu and Guang-Huey Lin
Microorganisms 2024, 12(2), 331; https://doi.org/10.3390/microorganisms12020331 - 4 Feb 2024
Viewed by 1235
Abstract
Background: Previous studies have confirmed the involvement of EmaSR (ethanol metabolism a sensor/regulator) in the regulation of Acinetobacter baumannii ATCC 19606 ethanol and acetate metabolism. RNA-seq analysis further revealed that DJ41_568-571, DJ41_2796, DJ41_3218, and DJ41_3568 regulatory gene clusters potentially participate [...] Read more.
Background: Previous studies have confirmed the involvement of EmaSR (ethanol metabolism a sensor/regulator) in the regulation of Acinetobacter baumannii ATCC 19606 ethanol and acetate metabolism. RNA-seq analysis further revealed that DJ41_568-571, DJ41_2796, DJ41_3218, and DJ41_3568 regulatory gene clusters potentially participate in ethanol and acetate metabolism under the control of EmaSR. Methods: This study fused the EmaSR regulon promoter segments with reporter genes and used fluorescence expression levels to determine whether EmaSR influences regulon expression in ethanol or acetate salt environments. The enzymatic function and kinetics of significantly regulated regulons were also studied. Results: The EmaSR regulons P2796 and P3218 exhibited > 2-fold increase in fluorescence expression in wild type compared to mutant strains in both ethanol and acetate environments, and PemaR demonstrated a comparable trend. Moreover, increases in DJ41_2796 concentration enhanced the conversion of acetate and succinyl-CoA into acetyl-CoA and succinate, suggesting that DJ41_2796 possesses acetate: succinyl-CoA transferase (ASCT) activity. The kcat/KM values for DJ41_2796 with potassium acetate, sodium acetate, and succinyl-CoA were 0.2131, 0.4547, and 20.4623 mM−1s−1, respectively. Conclusions: In A. baumannii, EmaSR controls genes involved in ethanol and acetate metabolism, and the EmaSR regulon DJ41_2796 was found to possess ASCT activity. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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19 pages, 3829 KiB  
Article
Regulatory Role of GgaR (YegW) for Glycogen Accumulation in Escherichia coli K-12
by Shunsuke Saito, Ikki Kobayashi, Motoki Hoshina, Emi Uenaka, Atsushi Sakurai, Sousuke Imamura and Tomohiro Shimada
Microorganisms 2024, 12(1), 115; https://doi.org/10.3390/microorganisms12010115 - 5 Jan 2024
Viewed by 2071
Abstract
Glycogen, the stored form of glucose, accumulates upon growth arrest in the presence of an excess carbon source in Escherichia coli and other bacteria. Chromatin immunoprecipitation screening for the binding site of a functionally unknown GntR family transcription factor, YegW, revealed that the [...] Read more.
Glycogen, the stored form of glucose, accumulates upon growth arrest in the presence of an excess carbon source in Escherichia coli and other bacteria. Chromatin immunoprecipitation screening for the binding site of a functionally unknown GntR family transcription factor, YegW, revealed that the yegTUV operon was a single target of the E. coli genome. Although none of the genes in the yegTUV operon have a clear function, a previous study suggested their involvement in the production of ADP-glucose (ADPG), a glycogen precursor. Various validation through in vivo and in vitro experiments showed that YegW is a single-target transcription factor that acts as a repressor of yegTUV, with an intracellular concentration of consistently approximately 10 molecules, and senses ADPG as an effector. Further analysis revealed that YegW repressed glycogen accumulation in response to increased glucose concentration, which was not accompanied by changes in the growth phase. In minimal glucose medium, yegW-deficient E. coli promoted glycogen accumulation, at the expense of poor cell proliferation. We concluded that YegW is a single-target transcription factor that senses ADPG and represses glycogen accumulation in response to the amount of glucose available to the cell. We propose renaming YegW to GgaR (repressor of glycogen accumulation). Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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18 pages, 8358 KiB  
Article
Regulatory Functions of PurR in Yersinia pestis: Orchestrating Diverse Biological Activities
by Liting Xiao, Junyan Jin, Kai Song, Xiuwei Qian, Yarong Wu, Zhulin Sun, Ziyao Xiong, Yanbing Li, Yanting Zhao, Leiming Shen, Yiming Cui, Wenwu Yao, Yujun Cui and Yajun Song
Microorganisms 2023, 11(11), 2801; https://doi.org/10.3390/microorganisms11112801 - 17 Nov 2023
Viewed by 1377
Abstract
The bacterium Yersinia pestis has developed various strategies to sense and respond to the complex stresses encountered during its transmission and pathogenic processes. PurR is a common transcriptional regulator of purine biosynthesis among microorganisms, and it modulates the transcription level of the pur [...] Read more.
The bacterium Yersinia pestis has developed various strategies to sense and respond to the complex stresses encountered during its transmission and pathogenic processes. PurR is a common transcriptional regulator of purine biosynthesis among microorganisms, and it modulates the transcription level of the pur operon to suppress the production of hypoxanthine nucleotide (IMP). This study aims to understand the functions and regulatory mechanisms of purR in Y. pestis. Firstly, we constructed a purR knockout mutant of Y. pestis strain 201 and compared certain phenotypes of the null mutant (201-ΔpurR) and the wild-type strain (201-WT). The results show that deleting purR has no significant impact on the biofilm formation, growth rate, or viability of Y. pestis under different stress conditions (heat and cold shock, high salinity, and hyperosmotic pressure). Although the cytotoxicity of the purR knockout mutant on HeLa and 293 cells is reduced, the animal-challenging test found no difference of the virulence in mice between 201-ΔpurR and 201-WT. Furthermore, RNA-seq and EMSA analyses demonstrate that PurR binds to the promoter regions of at least 15 genes in Y. pestis strain 201, primarily involved in purine biosynthesis, along with others not previously observed in other bacteria. Additionally, RNA-seq results suggest the presence of 11 potential operons, including a newly identified co-transcriptional T6SS cluster. Thus, aside from its role as a regulator of purine biosynthesis, purR in Y. pestis may have additional regulatory functions. Full article
(This article belongs to the Special Issue Transcriptional Regulation in Bacteria)
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