Transcription–replication interactions reveal bacterial genome regulation

0
17
  • Bervoets, I. & Charlier, D. Diversity, versatility and complexity of bacterial gene regulation mechanisms: opportunities and drawbacks for applications in synthetic biology. FEMS Microbiol. Rev. 43, 304–339 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vilar, J. M. G., Guet, C. C. & Leibler, S. Modeling network dynamics: the lac operon, a case study. J. Cell Biol. 161, 471–476 (2003).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Narula, J., Devi, S. N., Fujita, M. & Igoshin, O. A. Ultrasensitivity of the Bacillus subtilis sporulation decision. Proc. Natl Acad. Sci. USA 109, E3513–E3522 (2012).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Homberger, C., Hayward, R. J., Barquist, L. & Vogel, J. Improved bacterial single-cell RNA-seq through automated MATQ-seq and Cas9-based removal of rRNA reads. mBio 14, e0355722 (2023).

    PubMed 

    Google Scholar
     

  • Balakrishnan, R. et al. Principles of gene regulation quantitatively connect DNA to RNA and proteins in bacteria. Science 378, eabk2066 (2022).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cooper, S. & Helmstetter, C. E. Chromosome replication and the division cycle of Escherichia coli B/r. J. Mol. Biol. 31, 519–540 (1968).

    CAS 
    PubMed 

    Google Scholar
     

  • Schaechter, M., Bentzon, M. W. & Maaloe, O. Synthesis of deoxyribonucleic acid during the division cycle of bacteria. Nature 183, 1207–1208 (1959).

    CAS 
    PubMed 

    Google Scholar
     

  • Wang, M., Zhang, J., Xu, H. & Golding, I. Measuring transcription at a single gene copy reveals hidden drivers of bacterial individuality. Nat. Microbiol. 4, 2118–2127 (2019).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Narula, J. et al. Chromosomal arrangement of phosphorelay genes couples sporulation and DNA replication. Cell 162, 328–337 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Slager, J. & Veening, J.-W. Hard-wired control of bacterial processes by chromosomal gene location. Trends Microbiol. 24, 788–800 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Peterson, J. R., Cole, J. A., Fei, J., Ha, T. & Luthey-Schulten, Z. A. Effects of DNA replication on mRNA noise. Proc. Natl Acad. Sci. USA 112, 15886–15891 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Laub, M. T., McAdams, H. H., Feldblyum, T., Fraser, C. M. & Shapiro, L. Global analysis of the genetic network controlling a bacterial cell cycle. Science 290, 2144–2148 (2000).

    CAS 
    PubMed 

    Google Scholar
     

  • Fang, G. et al. Transcriptomic and phylogenetic analysis of a bacterial cell cycle reveals strong associations between gene co-expression and evolution. BMC Genom. 14, 450 (2013).


    Google Scholar
     

  • Zhou, B. et al. The global regulatory architecture of transcription during the Caulobacter cell cycle. PLoS Genet. 11, e1004831 (2015).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • De Nisco, N. J., Abo, R. P., Wu, C. M., Penterman, J. & Walker, G. C. Global analysis of cell cycle gene expression of the legume symbiont Sinorhizobium meliloti. Proc. Natl Acad. Sci. USA 111, 3217–3224 (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bandekar, A. C., Subedi, S., Ioerger, T. R. & Sassetti, C. M. Cell-cycle-associated expression patterns predict gene function in Mycobacteria. Curr. Biol. 30, 3961–3971.e6 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cooper, S. The synchronization manifesto: a critique of whole-culture synchronization. FEBS J. 286, 4650–4656 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • Blattman, S. B., Jiang, W., Oikonomou, P. & Tavazoie, S. Prokaryotic single-cell RNA sequencing by in situ combinatorial indexing. Nat. Microbiol. 5, 1192–1201 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kuchina, A. et al. Microbial single-cell RNA sequencing by split-pool barcoding. Science 371, eaba5257 (2021).

    CAS 
    PubMed 

    Google Scholar
     

  • Imdahl, F., Vafadarnejad, E., Homberger, C., Saliba, A.-E. & Vogel, J. Single-cell RNA-sequencing reports growth-condition-specific global transcriptomes of individual bacteria. Nat. Microbiol. 5, 1202–1206 (2020).

    CAS 
    PubMed 

    Google Scholar
     

  • Homberger, C., Barquist, L. & Vogel, J. Ushering in a new era of single-cell transcriptomics in bacteria. microLife 3, uqac020 (2022).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lopez, R., Regier, J., Cole, M. B., Jordan, M. I. & Yosef, N. Deep generative modeling for single-cell transcriptomics. Nat. Methods 15, 1053–1058 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bremer, H. & Dennis, P. P. Modulation of chemical composition and other parameters of the cell at different exponential growth rates. EcoSal Plus 3, (2008).

  • Michelsen, O., Teixeira de Mattos, M. J., Jensen, P. R. & Hansen, F. G. Precise determinations of C and D periods by flow cytometry in Escherichia coli K-12 and B/r. Microbiology 149, 1001–1010 (2003).

    CAS 
    PubMed 

    Google Scholar
     

  • Wang, X., Lesterlin, C., Reyes-Lamothe, R., Ball, G. & Sherratt, D. J. Replication and segregation of an Escherichia coli chromosome with two replication origins. Proc. Natl Acad. Sci. USA 108, E243–E250 (2011).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dimude, J. U. et al. Origins left, right, and centre: increasing the number of initiation sites in the chromosome. Genes 9, 376 (2018).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ivanova, D. et al. Shaping the landscape of the Escherichia coli chromosome: replication-transcription encounters in cells with an ectopic replication origin. Nucleic Acids Res. 43, 7865–7877 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khodursky, A. B. et al. Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc. Natl Acad. Sci. USA 97, 9419–9424 (2000).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pham, T. M. et al. A single-molecule approach to DNA replication in Escherichia coli cells demonstrated that DNA polymerase III is a major determinant of fork speed. Mol. Microbiol. 90, 584–596 (2013).

    CAS 
    PubMed 

    Google Scholar
     

  • Kjeldgaard, N. O., Maaloe, O. & Schaechter, M. The transition between different physiological states during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19, 607–616 (1958).

    CAS 
    PubMed 

    Google Scholar
     

  • Skinner, S. O., Sepúlveda, L. A., Xu, H. & Golding, I. Measuring mRNA copy number in individual Escherichia coli cells using single-molecule fluorescent in situ hybridization. Nat. Protoc. 8, 1100–1113 (2013).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Proshkin, S., Rahmouni, A. R., Mironov, A. & Nudler, E. Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328, 504–508 (2010).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pomerantz, R. T. & O’Donnell, M. The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456, 762–766 (2008).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • de la Fuente, A., Palacios, P. & Vicente, M. Transcription of the Escherichia coli dcw cluster: evidence for distal upstream transcripts being involved in the expression of the downstream ftsZ gene. Biochimie 83, 109–115 (2001).

    PubMed 

    Google Scholar
     

  • Flärdh, K., Palacios, P. & Vicente, M. Cell division genes ftsQAZ in Escherichia coli require distant cis-acting signals upstream of ddlB for full expression. Mol. Microbiol. 30, 305–315 (1998).

    PubMed 

    Google Scholar
     

  • Lutkenhaus, J. F., Wolf-Watz, H. & Donachie, W. D. Organization of genes in the ftsA–envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J. Bacteriol. 142, 615–620 (1980).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zaslaver, A., Mayo, A., Ronen, M. & Alon, U. Optimal gene partition into operons correlates with gene functional order. Phys. Biol. 3, 183–189 (2006).

    CAS 
    PubMed 

    Google Scholar
     

  • Zhu, M., Mu, H., Han, F., Wang, Q. & Dai, X. Quantitative analysis of asynchronous transcription–translation and transcription processivity in under various growth conditions. iScience 24, 103333 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhu, M., Mori, M., Hwa, T. & Dai, X. Disruption of transcription–translation coordination in Escherichia coli leads to premature transcriptional termination. Nat. Microbiol. 4, 2347–2356 (2019).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sharpe, M. E., Hauser, P. M., Sharpe, R. G. & Errington, J. Bacillus subtilis cell cycle as studied by fluorescence microscopy: constancy of cell length at initiation of DNA replication and evidence for active nucleoid partitioning. J. Bacteriol. 180, 547–555 (1998).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Golding, I. Revisiting replication-induced transcription in Escherichia coli. Bioessays 42, e1900193 (2020).

    PubMed 

    Google Scholar
     

  • Guptasarma, P. Does replication-induced transcription regulate synthesis of the myriad low copy number proteins of Escherichia coli? Bioessays 17, 987–997 (1995).

    CAS 
    PubMed 

    Google Scholar
     

  • Ray, A., Edmonds, K. A., Palmer, L. D., Skaar, E. P. & Giedroc, D. P. Glucose-induced biofilm accessory protein A (GbaA) is a monothiol-dependent electrophile sensor. Biochemistry 59, 2882–2895 (2020).

    CAS 
    PubMed 

    Google Scholar
     

  • Van Loi, V. et al. The two-Cys-type TetR repressor GbaA confers resistance under disulfide and electrophile stress in Staphylococcus aureus. Free Radic. Biol. Med. 177, 120–131 (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Campbell, J. L. & Kleckner, N. E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62, 967–979 (1990).

    CAS 
    PubMed 

    Google Scholar
     

  • Theisen, P. W., Grimwade, J. E., Leonard, A. C., Bogan, J. A. & Helmstetter, C. E. Correlation of gene transcription with the time of initiation of chromosome replication in Escherichia coli. Mol. Microbiol. 10, 575–584 (1993).

    CAS 
    PubMed 

    Google Scholar
     

  • Buettner, F. et al. Computational analysis of cell-to-cell heterogeneity in single-cell RNA-sequencing data reveals hidden subpopulations of cells. Nat. Biotechnol. 33, 155–160 (2015).

    CAS 
    PubMed 

    Google Scholar
     

  • Cooper, S. The Escherichia coli cell cycle. Res. Microbiol. 141, 17–29 (1990).

    CAS 
    PubMed 

    Google Scholar
     

  • Garrido, T., Sánchez, M., Palacios, P., Aldea, M. & Vicente, M. Transcription of ftsZ oscillates during the cell cycle of Escherichia coli. EMBO J. 12, 3957–3965 (1993).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhou, P. & Helmstetter, C. E. Relationship between ftsZ gene expression and chromosome replication in Escherichia coli. J. Bacteriol. 176, 6100–6106 (1994).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lin, J. & Amir, A. Homeostasis of protein and mRNA concentrations in growing cells. Nat. Commun. 9, 4496 (2018).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rosenfeld, N., Elowitz, M. B. & Alon, U. Negative autoregulation speeds the response times of transcription networks. J. Mol. Biol. 323, 785–793 (2002).

    CAS 
    PubMed 

    Google Scholar
     

  • Ma, P. et al. Bacterial droplet-based single-cell RNA-seq reveals antibiotic-associated heterogeneous cellular states. Cell 186, 877–891.e14 (2023).

    CAS 
    PubMed 

    Google Scholar
     

  • Brennan, M. A. & Rosenthal, A. Z. Single-Cell RNA sequencing elucidates the structure and organization of microbial communities. Front. Microbiol. 12, 713128 (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu, Z. et al. Droplet-based high-throughput single microbe RNA sequencing by smRandom-seq. Nat. Commun. 14, 5130 (2023).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Luecken, M. D. & Theis, F. J. Current best practices in single-cell RNA-seq analysis: a tutorial. Mol. Syst. Biol. 15, e8746 (2019).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jun, S., Si, F., Pugatch, R. & Scott, M. Fundamental principles in bacterial physiology-history, recent progress, and the future with focus on cell size control: a review. Rep. Prog. Phys. 81, 056601 (2018).

    MathSciNet 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • La Manno, G. et al. RNA velocity of single cells. Nature 560, 494–498 (2018).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bergen, V., Soldatov, R. A., Kharchenko, P. V. & Theis, F. J. RNA velocity-current challenges and future perspectives. Mol. Syst. Biol. 17, e10282 (2021).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wolf, F. A., Angerer, P. & Theis, F. J. SCANPY: large-scale single-cell gene expression data analysis. Genome Biol. 19, 15 (2018).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arndt, D. et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 44, W16–W21 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Levin, M. et al. The mid-developmental transition and the evolution of animal body plans. Nature 531, 637–641 (2016).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zalts, H. & Yanai, I. Developmental constraints shape the evolution of the nematode mid-developmental transition. Nat. Ecol. Evol. 1, 113 (2017).

    PubMed 

    Google Scholar
     

  • Keseler, I. M. et al. The EcoCyc database in 2021. Front. Microbiol. 12, 711077 (2021).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Karp, P. D. et al. The BioCyc collection of microbial genomes and metabolic pathways. Brief. Bioinform. 20, 1085–1093 (2019).

    CAS 
    PubMed 

    Google Scholar
     

  • Fuchs, S. et al. AureoWiki—the repository of the Staphylococcus aureus research and annotation community. Int. J. Med. Microbiol. 308, 558–568 (2018).

    PubMed 

    Google Scholar
     

  • Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17, 261–272 (2020).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen, J., Yoong, P., Ram, G., Torres, V. J. & Novick, R. P. Single-copy vectors for integration at the SaPI1 attachment site for Staphylococcus aureus. Plasmid 76, 1–7 (2014).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Benson, M. A. et al. Staphylococcus aureus regulates the expression and production of the staphylococcal superantigen-like secreted proteins in a Rot-dependent manner. Mol. Microbiol. 81, 659–675 (2011).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • LEAVE A REPLY

    Please enter your comment!
    Please enter your name here