Morigen
Monika Glinkowska
Jianping Xie
Richa Priyadarshini
Kazutoshi Kasho- 1State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, School of Life Sciences, Inner Mongolia University, Hohhot, China
- 2Department of Bacterial Molecular Genetics, University of Gdansk, Gdańsk, Poland
- 3Institute of Modern Biopharmaceuticals, School of Life Sciences, Southwest University, Chongqing, China
- 4Department of Life Sciences, School of Natural Science, Shiv Nadar Institution of Eminence, Gautam Buddha Nagar, India
- 5Department of Molecular Biology, Graduate School of Pharmaceutical Sciences, Kyushu University, Fukuoka, Japan
Editorial on the Research Topic
Bacterial transcription factors and the cell cycle, volume II
The progression of the bacterial cell cycle is a result of the fluctuation in gene expression regulated by transcription factors. It is well-known that the initiator protein DnaA controls gene expression as a transcription factor (Messer and Weigel, 1997) while it triggers the initiation of DNA replication (Fuller and Kornberg, 1983). Thus, it is reasonable to assume that dual functional DnaA temporally and spatially coordinates different cellular pathways with the initiation of DNA replication. Indeed, in Caulobacter crescentus, DnaA couples chromosome replication with the expression of GcrA and CtrA, which are two important oscillating regulators. The regulatory cascade made of DnaA/GcrA/CtrA pushes forward the succession of the cell cycle coordinately (Collier et al., 2006). As reviewed recently (Menikpurage et al., 2021), DnaA might be involved in the development of different cellular events of quorum sensing, cell motility, DNA repair (Wurihan et al., 2018), and cell cycle control by regulating the expression of the genes associated. Most recently, DnaA was reported to regulate transcription attenuation of the his operon (Yao et al., 2023). Other transcription factors, for example, RpoS in Coxiella controls the expression of the developmental cycle genes (Moormeier et al., 2019), and BolA in the Gram-negative bacteria turns on biofilm development while it turns off motility as a transcription factor (Dressaire et al., 2015). In Volume I of the Research Topic (Morigen et al., 2021), the following studies were included: (i) functional identification of transcription factors Mfd, DagR, RsbW homologs, Crp1, OxyR, and NprR in various bacteria; (ii) determination of histone-like nucleoid-binding protein YbaBCc and genome-wide cell cycle-dependent binding patterns of IHF to chromosome with base-pair resolution using GeF-seq; (iii) direct interaction and function of ZapE with FtsZ in cell division and the DnaA (L366K)-mediated restoration of growth defect due to the accumulation of lipoprotein Lpp (C21G). Also, the orisome assembling and function in each cell cycle and the conserved location of CtrA phosphorelay associated genes to ori and ter of the bacterial circular chromosome were described. Volume II of the Research Topic is also a collection of articles focusing on the bacterial transcription factors and the cell cycle, particularly transcription factors, transcription, and cell division.
Transcription factors and transcription
The OmpR protein is a transcription factor and also a part of the EnvZ/OmpR two-component system (TCS), which has been shown to be involved in prodigiosin biosynthesis. Prodigiosin is a secondary metabolite that has various pharmacological activities. Prodigiosin production has been found in some bacteria and is largely produced in Serratia marcescens. The biosynthesis of prodigiosin in S. marcescens is affected by temperature, pH, and medium composition and regulated by the EnvZ/OmpR system, which senses various environmental stress and growth conditions. Jia et al. showed that OmpR increased prodigiosin production in S. marcescens FZSF02. Further, in this study, OmpR was found to directly bind to the promoter regions of the pig gene cluster that is associated with prodigiosin biosynthesis and of the envZ/ompR genes. The authors also found that the 5′CATTTATTTACATTTAC3′ sequence in the pig promoter was the binding target of OmpR by DNase I footprinting assay. The work concludes that OmpR regulates its own expression and the pig gene cluster, and subsequently governs the production of prodigiosin in S. marcescens, being a transcription factor. Another transcription factor, Ste12, has been shown to regulate stress tolerance and sexual reproduction in fungi. Lyu et al. constructed the phylogenetic tree of Ste12-like proteins of Flammulina filiformis and other fungi by comparison of the amino acid sequences and showed that the Ste12-like proteins contained the conserved amino acid sequences with three typical motifs, namely, motif 1, 2, and 3. Subsequently, using Agrobacterium tumefaciens-mediated transformation, Lyu et al. constructed four ste12-like overexpression transformants of F. filiformis, and it was found that these overexpression transformants were more tolerant to salt, cold, and oxidative stress with an increased number of fruiting bodies but at a slow growth rate. The results allow the authors to conclude that the Ste12-like protein participates in the regulation of abiotic stress tolerance and fruiting body development in F. filiformis.
Interestingly, in the WalK/WalR two-component system of Streptococcus mutans, Kong et al. found that the histidine kinase WalK had an extended C-terminal tail (CTT) in 14 different TCSs, and CTT plays a crucial role in the interaction of WalK with its response regulator WalR, a transcription factor. It was demonstrated that the tryptophan in CTT was required for WalK signaling since W443 in the CTT is essential for the phosphotransferase and phosphatase activities of WalK. Any mutation which disrupts the interaction of WalK with WalR in CTT might impair the signaling processes of this TCS. The tryptophan was also shown to be key for WalK to compete with a DNA that contains a WalR binding motif and is important for transcription control in vivo and biofilm formation. Similarly, the Staphylococcus aureus WalK has a remarkable CTT although it is short in length; it possesses a conserved W-acidic motif. In conclusion, the W-acidic motif in WalK is essential for the WalK-WalR interaction, playing a key role in the WalR/WalK-dependent signal transduction, biofilm formation, and transcription regulation. It should be noted that a transcriptome analysis on an isolate of Cellulomonas fimi from polluted river water, strain Clb-11, is interesting. The Clb-11 strain could generate electricity in microbial fuel cells with carboxymethyl cellulose as the carbon source and secrete chromate reductase or electron mediator to reduce Cr (VI) to Cr (III). To understand how the Clb-11 strain reduces Cr (VI) to Cr (III), Cao et al. analyzed differentially-expressed genes involved in different Cr (VI) stress responses in Clb-11 by RNA-sequencing and found that 99 genes were up-regulated while 78 genes were down-regulated as the Cr (VI) concentration increased. The differentially-expressed genes are mainly associated with DNA repair, ABC transporters, amino sugar, and carbon metabolism to cope with Cr (VI) stress-induced DNA damage and cellular toxic effect. The work may provide clues to understanding the molecular mechanism of Cr (VI) reduction in the Clb-11 strain.
Cell division
Bacterial cell division is a highly regulated molecular process in which the conserved tubulin homolog FtsZ assembles into the Z-ring at mid-cell on the interior of the cell membrane through polymerization. The FtsZ polymers recruit FtsA in Escherichia coli, a membrane-associated protein, by directly interacting with it. FtsA polymerizes into an actin-like structure, promoted by ATP binding, displaying considerable flexibility in conformation across different nucleotide-bound states. Morrison et al. showed that several amino acid residues near the nucleotide-binding site in FtsA were key for function, being associated with ATP hydrolysis, phospholipid (PL) binding, ATP-dependent vesicle remodeling, and recruitment to the divisome in vivo. For example, Ser-84 and Glu-14 residues in FtsA are essential for ATP-dependent vesicle remodeling and magnesium-dependent membrane release of FtsA from vesicles in vitro; FtsA (A188V) is defective for rapid ATP hydrolysis and ATP-dependent remodeling of PL vesicles in vitro. The work concludes that nucleotide-dependent activities of FtsA regulate the early establishment of a functional divisome during the E. coli cell cycle.
Author contributions
M and JX wrote the first manuscript draft. M edited the final version. All authors listed have made a substantial, direct, and intellectual contribution to the work, revised, and approved it for publication.
Funding
This work was supported by grants from the National Natural Science Foundation of China NSFC (Grant no. 32260233 to M) and the Inner Mongolia Key Laboratory for Molecular Regulation of the Cell (Grant no. 2021PT0002 to M).
Acknowledgments
We sincerely thank all the authors and reviewers who have participated in this Research Topic.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Collier, J., Murray, S. R., and Shapiro, L. (2006). DnaA couples DNA replication and the expression of two cell cycle master regulators. Embo J. 25, 346–356. doi: 10.1038/sj.emboj.7600927
Dressaire, C., Moreira, R. N., Barahona, S., Alves De Matos, A. P., and Arraiano, C. M. (2015). BolA is a transcriptional switch that turns off motility and turns on biofilm development. mBio 6, e02352–02314. doi: 10.1128/mBio.02352-14
Fuller, R. S., and Kornberg, A. (1983). Purified dnaA protein in initiation of replication at the Escherichia coli chromosomal origin of replication. Proc. Natl. Acad. Sci. U S A. 80, 5817–5821. doi: 10.1073/pnas.80.19.5817
Menikpurage, I. P., Woo, K., and Mera, P. E. (2021). Transcriptional activity of the bacterial replication initiator DnaA. Front. Microbiol. 12, 662317. doi: 10.3389/fmicb.2021.662317
Messer, W., and Weigel, C. (1997). DnaA initiator–also a transcription factor. Mol. Microbiol. 24, 1–6. doi: 10.1046/j.1365-2958.1997.3171678.x
Moormeier, D. E., Sandoz, K. M., Beare, P. A., Sturdevant, D. E., Nair, V., Cockrell, D. C., et al. (2019). Coxiella burnetii RpoS regulates genes involved in morphological differentiation and intracellular growth. J. Bacteriol. 4, 201. doi: 10.1128/JB.00009-19
Morigen, Glinkowska, M., and Xie, J. (2021). Editorial: bacterial transcription factors and the cell cycle. Front Microbiol. 12, 821394. doi: 10.3389/fmicb.2021.821394
Wurihan Gezi Brambilla, E., Wang, S., Sun, H., Fan, L., Shi, Y., Sclavi, B., and Morigen (2018). DnaA and LexA proteins regulate transcription of the uvrB Gene in Escherichia coli: the role of DnaA in the control of the SOS regulon. Front. Microbiol .9, 1212. doi: 10.3389/fmicb.2018.01212
Keywords: bacteria, transcription factor, transcription, signaling, cell division
Citation: Morigen, Glinkowska M, Xie J, Priyadarshini R and Kasho K (2023) Editorial: Bacterial transcription factors and the cell cycle, volume II. Front. Microbiol. 14:1252924. doi: 10.3389/fmicb.2023.1252924
Received: 04 July 2023; Accepted: 13 July 2023;
Published: 25 July 2023.
Edited and reviewed by: Sabine Kleinsteuber, Helmholtz Association of German Research Centres (HZ), Germany
Copyright © 2023 Morigen, Glinkowska, Xie, Priyadarshini and Kasho. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Morigen, bW9yaWdlbm0mI3gwMDA0MDtob3RtYWlsLmNvbQ==; Jianping Xie, Z2VvcmdleCYjeDAwMDQwO3N3dS5lZHUuY24=