Defined chromosome structure in the genome-reduced bacterium Mycoplasma pneumoniae
Open accessAbstract
DNA-binding proteins are central regulators of chromosome organization; however, in genome-reduced bacteria their diversity is largely diminished. Whether the chromosomes of such bacteria adopt defined three-dimensional structures remains unexplored. Here we combine Hi-C and super-resolution microscopy to determine the structure of the Mycoplasma pneumoniae chromosome at a 10 kb resolution. We find a defined structure, with a global symmetry between two arms that connect opposite poles, one bearing the chromosomal Ori and the other the midpoint. Analysis of local structures at a 3 kb resolution indicates that the chromosome is organized into domains ranging from 15 to 33 kb. We provide evidence that genes within the same domain tend to be co-regulated, suggesting that chromosome organization influences transcriptional regulation, and that supercoiling regulates local organization. This study extends the current understanding of bacterial genome organization and demonstrates that a defined chromosomal structure is a universal feature of living systems.
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In Mycoplasma pneumoniae, super-resolution imaging suggests anchoring of the Ter-proximal region of the DNA to the attachment organelle.
“In Mycoplasma pneumoniae, super-resolution imaging suggests anchoring of the Ter-proximal region of the DNA to the attachment organelle.84”
From Bringing the genetically minimal cell to life on a computer in 4D (2026) · cites this paper as [84]
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References 72 · Cited by 114
Research works printed but not linked: 62
- Cremer T. & Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2, 292– 301 (2001). 11283701
- Misteli T. Beyond the sequence: cellular organization of genome function. Cell 128, 787– 800 (2007). 17320514
- Dorman C. J. Genome architecture and global gene regulation in bacteria: making progress towards a unified model? Nat. Rev. Microbiol. 11, 349– 355 (2013). 23549066
- Baranello L., Levens D., Gupta A. & Kouzine F. The importance of being supercoiled: how DNA mechanics regulate dynamic processes. Biochim. Biophys. Acta 1819, 632– 638 (2012). 22233557 PMC3354648
- Dillon S. C. & Dorman C. J. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nat. Rev. Microbiol. 8, 185– 195 (2010). 20140026
- Staczek P. & Higgins N. P. Gyrase and Topo IV modulate chromosome domain size in vivo. Mol. Microbiol. 29, 1435– 1448 (1998). 9781880
- Postow L., Hardy C. D., Arsuaga J. & Cozzarelli N. R. Topological domain structure of the Escherichia coli chromosome. Genes Dev. 18, 1766– 1779 (2004). 15256503 PMC478196
- Lakadamyali M. & Cosma M. P. Advanced microscopy methods for visualizing chromatin structure. FEBS Lett. 589, 3023– 3030 (2015). 25896023
- Rust M. J., Bates M. & Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Method 3, 793– 796 (2006). PMC2700296 16896339
- Betzig E.. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642– 1645 (2006). 16902090
- Hess S. T., Girirajan T. P. K. & Mason M. D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91, 4258– 4272 (2006). 16980368 PMC1635685
- Fölling J.. Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat. Methods 5, 943– 945 (2008). 18794861
- Dekker J., Rippe K., Dekker M. & Kleckner N. Capturing chromosome conformation. Science 295, 1306– 1311 (2002). 11847345
- Wang W., Li G.-W., Chen C., Xie X. S. & Zhuang X. Chromosome organization by a nucleoid-associated protein in live bacteria. Science 333, 1445– 1449 (2011). 21903814 PMC3329943
- Lieberman-Aiden E.. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289– 293 (2009). 19815776 PMC2858594
- Baù D. & Marti-Renom M. Structure determination of genomic domains by satisfaction of spatial restraints. Chromosome Res. 19, 25– 35 (2011). 21190133
- Umbarger M. A.. The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol. Cell 44, 252– 264 (2011). 22017872 PMC3874842
- Le T. B. K., Imakaev M. V., Mirny L. A. & Laub M. T. High-resolution mapping of the spatial organization of a bacterial chromosome. Science (New York, N.Y.) 342, 731– 734 (2013). PMC3927313 24158908
- Le Dily F.. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev. 28, 2151– 2162 (2014). 25274727 PMC4180976
- Cagliero C., Grand R. S., Jones M. B., Jin D. J. & O'Sullivan J. M. Genome conformation capture reveals that the Escherichia coli chromosome is organized by replication and transcription. Nucleic Acids Res. 41, 6058– 6071 (2013). 23632166 PMC3695519
- Marbouty M.. Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms. eLife 3, e03318 (2014). 25517076 PMC4381813
- Marbouty M.. Condensin- and replication-mediated bacterial chromosome folding and origin condensation revealed by hi-c and super-resolution imaging. Mol. Cell 59, 588– 602 (2015). 26295962
- Wang X.. Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis. Genes Dev. 29, 1661– 1675 (2015). 26253537 PMC4536313
- Espeli O., Mercier R. & Boccard F. DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol. Microbiol. 68, 1418– 1427 (2008). 18410497
- Perez-Rueda E. & Collado-Vides J. The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Res. 28, 1838– 1847 (2000). 10734204 PMC102813
- Helmann J. D. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46, 47– 110 (2002). 12073657
- Herrmann R. & Reiner B. Mycoplasma pneumoniae and Mycoplasma genitalium: a comparison of two closely related bacterial species. Curr. Opin. Microbiol. 1, 572– 579 (1998). 10066529
- Cameron A. D., Stoebel D. M. & Dorman C. J. DNA supercoiling is differentially regulated by environmental factors and FIS in Escherichia coli and Salmonella enterica. Mol. Microbiol. 80, 85– 101 (2011). 21276095
- Zhang W. & Baseman J. B. Transcriptional regulation of MG_149, an osmoinducible lipoprotein gene from Mycoplasma genitalium. Mol. Microbiol. 81, 327– 339 (2011). 21692875 PMC3196619
- Razin S., Yogev D. & Naot Y. Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 62, 1094– 1156 (1998). 9841667 PMC98941
- Seto S., Layh-Schmitt G., Kenri T. & Miyata M. Visualization of the attachment organelle and cytadherence proteins of Mycoplasma pneumoniae by immunofluorescence microscopy. J. Bacteriol. 183, 1621– 1630 (2001). 11160093 PMC95047
- Mouw K. W. & Rice P. A. Shaping the Borrelia burgdorferi genome: crystal structure and binding properties of the DNA-bending protein Hbb. Mol. Microbiol. 63, 1319– 1330 (2007). 17244195
- Sluijter M., Hoogenboezem T., Hartwig N. G. & Vink C. The Mycoplasma pneumoniae MPN229 gene encodes a protein that selectively binds single-stranded DNA and stimulates recombinase A-mediated DNA strand exchange. BMC Microbiol. 8, 167 (2008). 18831760 PMC2572620
- Das D.. Crystal structure of a novel single-stranded DNA binding protein from Mycoplasma pneumoniae. Proteins 67, 776– 782 (2007). 17348019
- Torres-Puig S., Broto A., Querol E., Pinol J. & Pich O. Q. A novel sigma factor reveals a unique regulon controlling cell-specific recombination in Mycoplasma genitalium. Nucleic Acids Res. 43, 4923– 4936 (2015). 25925568 PMC4446450
- Maier T.. Quantification of mRNA and protein and integration with protein turnover in a bacterium. Mol. Syst. Biol. 7, 511 (2011). 21772259 PMC3159969
- Lluch-Senar M.. Comprehensive methylome characterization of Mycoplasma genitalium and Mycoplasma pneumoniae at single-base resolution. PLoS Genet. 9, e1003191 (2013). 23300489 PMC3536716
- Lluch-Senar M.. Defining a minimal cell: essentiality of small ORFs and ncRNAs in a genome-reduced bacterium. Mol. Syst. Biol. 11, 780 (2015). 25609650 PMC4332154
- Hilbert H., Himmelreich R., Plagens H. & Herrmann R. Sequence analysis of 56 kb from the genome of the bacterium Mycoplasma pneumoniae comprising the dnaA region, the atp operon and a cluster of ribosomal protein genes. Nucleic Acids Res 24, 628– 639 (1996). 8604303 PMC145699
- Trussart M.. Assessing the limits of restraint-based 3D modeling of genomes and genomic domains. Nucleic Acids Res. 43, 3465– 3477 (2015). 25800747 PMC4402535
- Serra F., Baù D., Filion G. & Marti-Renom M. A. Structural features of the fly chromatin colors revealed by automatic three-dimensional modeling. Preprint at:. bioRxiv (2016).
- Heuser J. E. The origins and evolution of freeze-etch electron microscopy. J. Electron Microsc. (Tokyo) 60, S3– S29 (2011). 21844598 PMC3202940
- Gustafsson M. G.. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957– 4970 (2008). 18326650 PMC2397368
- Seto S. & Miyata M. Attachment organelle formation represented by localization of cytadherence proteins and formation of the electron-dense core in wild-type and mutant strains of Mycoplasma pneumoniae. J. Bacteriol. 185, 1082– 1091 (2003). 12533484 PMC142798
- Berlatzky I. A., Rouvinski A. & Ben-Yehuda S. Spatial organization of a replicating bacterial chromosome. Proc. Natl Acad Sci. USA 105, 14136– 14140 (2008). 18779567 PMC2544591
- Junier I., Unal E. B., Yus E., Lloréns-Rico V. & Serrano L. Insights into the mechanisms of basal coordination of transcription using a genome-reduced bacterium. Cell Syst. 2, 391– 401 (2016). 27237741 PMC4920955
- Gellert M., O'Dea M. H., Itoh T. & Tomizawa J. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc. Natl Acad. Sci. USA 73, 4474– 4478 (1976). 794878 PMC431506
- Balish M. F. & Krause D. C. Mycoplasmas: a distinct cytoskeleton for wall-less bacteria. J. Mol. Microbiol. Biotechnol. 11, 244– 255 (2006). 16983199
- Hasselbring B. M., Jordan J. L., Krause R. W. & Krause D. C. Terminal organelle development in the cell wall-less bacterium Mycoplasma pneumoniae. Proc. Natl Acad. Sci. USA 103, 16478– 16483 (2006). 17062751 PMC1637607
- Quinlan D. C. & Maniloff J. Membrane association of the deoxyribonucleic acid growing-point region in Mycoplasma gallisepticum. J. Bacteriol. 112, 1375– 1379 (1972). 4264449 PMC251573
- Lee P. S., Lin D. C., Moriya S. & Grossman A. D. Effects of the chromosome partitioning protein Spo0J (ParB) on oriC positioning and replication initiation in Bacillus subtilis. J. Bacteriol. 185, 1326– 1337 (2003). 12562803 PMC142880
- Toro E., Hong S. H., McAdams H. H. & Shapiro L. Caulobacter requires a dedicated mechanism to initiate chromosome segregation. Proc. Natl Acad. Sci. USA 105, 15435– 15440 (2008). 18824683 PMC2563096
- Nielsen H. J., Ottesen J. R., Youngren B., Austin S. J. & Hansen F. G. The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Mol. Microbiol. 62, 331– 338 (2006). 17020576
- Booker B. M., Deng S. & Higgins N. P. DNA topology of highly transcribed operons in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 78, 1348– 1364 (2010). 21143310
- Raeside C.. Large chromosomal rearrangements during a long-term evolution experiment with Escherichia coli. MBio 5, e01377– 14 (2014). 25205090 PMC4173774
- Noom M. C., Navarre W. W., Oshima T., Wuite G. J. & Dame R. T. H-NS promotes looped domain formation in the bacterial chromosome. Curr. Biol. 17, R913– R914 (2007). 17983565
- Needleman S. B. & Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48, 443– 453 (1970). 5420325
- Miyata M. & Petersen J. D. Spike structure at the interface between gliding mycoplasma mobile cells and glass surfaces visualized by rapid-freeze-and-fracture electron microscopy. J. Bacteriol. 186, 4382– 4386 (2004). 15205441 PMC421615
- Strauss M. P.. 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol. 10, e1001389 (2012). 22984350 PMC3439403
- Pengo T., Holden S. J. & Manley S. PALMsiever: a tool to turn raw data into results for single-molecule localization microscopy. Bioinformatics 31, 797– 798 (2015). 25362091 PMC4341069
- Ovesny M., Krizek P., Borkovec J., Svindrych Z. & Hagen G. M. ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics 30, 2389– 2390 (2014). 24771516 PMC4207427
- Rao S. S.. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665– 1680 (2014). 25497547 PMC5635824
- Authors
- Trussart, M., Yus, E., Martinez, S., Baù, D., Tahara, Y. O., Pengo, T., Widjaja, M., Kretschmer, S., Swoger, J., Djordjevic, S., Turnbull, L., Whitchurch, C., Miyata, M., Marti-Renom, M. A., Lluch-Senar, M., & Serrano, L.
- Affiliations
- Universitat Pompeu Fabra (ES)
- Barcelona Institute of Science and Technology (ES)
- Osaka City University (JP)
- University of Technology Sydney (AU)
- Max Planck Institute of Biochemistry (DE)
- ORCID
- Venue
- Nature Communications
- Published
- 2017-03-08
- Volume
- 8
- Issue
- 1
- Pages
- 14665-14665
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC5344976
- OpenAlex
- W2593043670
- Cited by
- 114
- References
- 72
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 16 · 2023: 11 · 2022: 8 · 2021: 17 · 2020: 10 · 2019: 13 · 2018: 15 · 2017: 7
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (publishedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- UTS ePRESS (University of Technology Sydney) (submittedVersion)
- Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion, cc-by)
- Funders
- Centres de Recerca de Catalunya
- European Commission (2007–2013, FP7 2007-2013, HORIZON2020, FP7/2007, 634942)
- Generalitat de Catalunya (634942)
- Ministerio de Economía y Competitividad (BIO2007‐61762, SEV‐2012‐0208, BFU2013-47736-P)
- Japan Society for the Promotion of Science (24117002, 24117001, 17H01544)
- Instituto de Salud Carlos III (PI10/01702, FP7/2007-2013)
- European Regional Development Fund (FP7/2007‐2013, 2007 – 2013)
- FP7 Ideas: European Research Council (232913, 609989)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- Mycoplasma pneumoniae, bacterial chromosome structure, genome reduction, DNA-binding proteins, chromosome organization, chromosomal domains, supercoiling, transcriptional regulation, Hi-C, super-resolution microscopy
- MeSH terms
- Chromosomes, Bacterial, DNA, Bacterial, DNA, Superhelical, Microscopy, Molecular Conformation, Mycoplasma pneumoniae, Nucleic Acid Conformation, Gene Expression Regulation, Bacterial, Genome, Bacterial, Chromosome Structures
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