TRR 174: Spatiotemporal dynamics of bacterial cells
Medicine
Final Report Abstract
Bacteria are ubiquitous in the environment and of great ecological, medical and biotechnological importance, thereby influencing many aspects of human life. Over the past three decades, new developments in methods and imaging technologies have enabled unprecedented insights into their cell biology. These advances have led to the realization that bacteria are highly organized entities in which individual components are precisely arranged within the cellular space. The localization patterns observed are often highly dynamic and change over time as a function of the cell cycle or in response to external cues. These spatiotemporal dynamics form the basis of essential cellular processes such as cell growth and division, DNA segregation, cell cycle regulation, cell differentiation, environmental interactions and motility. However, despite the considerable progress made in the field, it is still unclear how this dynamic spatial organization is accomplished and how it has evolved. The research groups within TRR 174 used a highly collaborative and interdisciplinary research approach to address these outstanding questions and comprehensively investigate the Spatiotemporal dynamics of bacterial cells. TRR 174 comprised 16 research groups from the Marburg and Munich areas, which all shared a common interest in bacterial cell biology but contributed complementary sets of expertise, ranging from molecular biology, cell biology and genetics over the biochemical, biophysical and structural characterization of proteins to mathematical modeling and synthetic biology. Building on this highly interdisciplinary background, the consortium investigated closely interconnected sets of spatiotemporally organized systems that critically contribute to the function of bacterial cells, with a focus on (i) cell growth, morphogenesis, and division, (ii) DNA organization, segregation and interactions, (iii) the positioning of motility structures and (iv) the assembly dynamics of membrane protein complexes. The central goal of these studies was to understand how local interactions between individual cellular components can give rise to the dynamic three-dimensional organization of bacterial cells. To this end, the consortium identified the components controlling central cellular processes, dissected their collective behavior in vivo and comprehensively analyze their properties and interactions in vitro. In a complementary approach, modeling studies were performed to unravel the emergent properties of the systems under investigation. Finally, reconstitution studies of isolated systems were used as a means to test for the completeness of the understanding gained. Importantly, the research conducted in TRR 174 involved a range of different bacterial model organisms. By studying a defined set of cellular processes in evolutionarily distinct species, it was possible to determine whether spatiotemporally organized systems mediating particular cellular processes relied on similar design principles. Moreover, this comparative approach helped to identify different solutions that nature has evolved to perform given cellular tasks. In the long run, the results obtained by TRR 174 may contribute to the identification of new antibiotic targets or provide the basis for the design of synthetic spatiotemporally organized systems to optimize cells for applied purposes. Altogether, the findings made by TRR 174 led to 104 research papers in internationally renowned and peer-reviewed scientific journals. Importantly, 35 publications resulted from collaborative projects conducted by two or more research groups. To facilitate the exchange of results and ideas with the international scientific community, TRR 174 hosted 58 internationally renowned scientists, who gave guess lectures on cutting-edge findings in the research fields covered by the consortium. Moreover, it organized two large international conferences in the field of bacterial cell biology and provided organizational and financial support for various other scientific symposia, workshops and summer schools. TRR 174 also participated in a variety of outreach activities to convey its findings to the general public. The collaborative work of TRR 174 was facilitated by comprehensive support structures that fostered interactions among the participating research groups and promoted the development of early-career researchers into independent scientists ready to take the next steps of their professional career. In total, 47 doctoral candidates conducted their thesis work in the framework of TRR 174, with a balanced gender ratio (47% female). Their advanced training was ensured by a series of activities, including guest lectures, progress seminars, retreats, scientific and transferable-skills workshops and industry visits. Gender equality and family friendliness were promoted through various support measures, gender awareness workshops and counseling sessions specifically tailored to the needs of female scientists. Collectively, the activities of TRR 174 made an important contribution to understanding the mechanisms that govern the spatiotemporal dynamics of cellular processes in bacteria. The consortium has left a highly visible footprint in its research field, fostered a new generation of critically thinking, broadly trained scientists, and laid a solid foundation for continuous close collaborations among the participating research groups.
Publications
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A Family of Single Copy repABC-Type Shuttle Vectors Stably Maintained in the Alpha-Proteobacterium Sinorhizobium meliloti. ACS Synthetic Biology, 6(6), 968-984.
Döhlemann, Johannes; Wagner, Marcel; Happel, Carina; Carrillo, Martina; Sobetzko, Patrick; Erb, Tobias J.; Thanbichler, Martin & Becker, Anke
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Bactofilin-mediated organization of the ParABS chromosome segregation system in Myxococcus xanthus. Nature Communications, 8(1).
Lin, Lin; Osorio, Valeriano Manuel; Harms, Andrea; Søgaard-Andersen, Lotte & Thanbichler, Martin
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The PomXYZ Proteins Self-Organize on the Bacterial Nucleoid to Stimulate Cell Division. Developmental Cell, 41(3), 299-314.e13.
Schumacher, Dominik; Bergeler, Silke; Harms, Andrea; Vonck, Janet; Huneke-Vogt, Sabrina; Frey, Erwin & Søgaard-Andersen, Lotte
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Beating Vesicles: Encapsulated Protein Oscillations Cause Dynamic Membrane Deformations. Angewandte Chemie International Edition, 57(50), 16286-16290.
Litschel, Thomas; Ramm, Beatrice; Maas, Roel; Heymann, Michael & Schwille, Petra
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Regulation of Pom cluster dynamics in Myxococcus xanthus. PLOS Computational Biology, 14(8), e1006358.
Bergeler, Silke & Frey, Erwin
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Single molecule tracking reveals that the bacterial SMC complex moves slowly relative to the diffusion of the chromosome. Nucleic Acids Research, 46(15), 7805-7819.
Schibany, Sonja; KleineBorgmann, Luise A. K.; Rösch, Thomas C.; Knust, Tobias; Ulbrich, Maximilian H. & Graumann, Peter L.
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The MinDE system is a generic spatial cue for membrane protein distribution in vitro. Nature Communications, 9(1).
Ramm, Beatrice; Glock, Philipp; Mücksch, Jonas; Blumhardt, Philipp; García-Soriano, Daniela A.; Heymann, Michael & Schwille, Petra
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Transmembrane region of bacterial chemoreceptor is capable of promoting protein clustering. Journal of Biological Chemistry, 293(6), 2149-2158.
Pollard, Abiola M. & Sourjik, Victor
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ZomB is essential for flagellar motor reversals in Shewanella putrefaciens and Vibrio parahaemolyticus. Molecular Microbiology, 109(5), 694-709.
Brenzinger, Susanne; Pecina, Anna; Mrusek, Devid; Mann, Petra; Völse, Kerstin; Wimmi, Stephan; Ruppert, Ulrike; Becker, Anke; Ringgaard, Simon; Bange, Gert & Thormann, Kai M.
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Can a Flux-Based Mechanism Explain Protein Cluster Positioning in a Three-Dimensional Cell Geometry?. Biophysical Journal, 117(3), 420-428.
Kober, Matthias; Bergeler, Silke & Frey, Erwin
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DNA-binding directs the localization of a membrane-integrated receptor of the ToxR family. Communications Biology, 2(1).
Brameyer, Sophie; Rösch, Thomas C.; El Andari, Jihad; Hoyer, Elisabeth; Schwarz, Julia; Graumann, Peter L. & Jung, Kirsten
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ParB-type DNA Segregation Proteins Are CTP-Dependent Molecular Switches. Cell, 179(7), 1512-1524.e15.
Osorio-Valeriano, Manuel; Altegoer, Florian; Steinchen, Wieland; Urban, Svenja; Liu, Ying; Bange, Gert & Thanbichler, Martin
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Spatial control of the GTPase MglA by localized RomR–RomX GEF and MglB GAP activities enables Myxococcus xanthus motility. Nature Microbiology, 4(8), 1344-1355.
Szadkowski, Dobromir; Harms, Andrea; Carreira, Luis António Menezes; Wigbers, Manon; Potapova, Anna; Wuichet, Kristin; Keilberg, Daniela; Gerland, Ulrich & Søgaard-Andersen, Lotte
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Substrate‐dependent cluster density dynamics of Corynebacterium glutamicum phosphotransferase system permeases. Molecular Microbiology, 111(5), 1335-1354.
Martins, Gustavo Benevides; Giacomelli, Giacomo; Goldbeck, Oliver; Seibold, Gerd M. & Bramkamp, Marc
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Symmetric activity of DNA polymerases at and recruitment of exonuclease ExoR and of PolA to the Bacillus subtilis replication forks. Nucleic Acids Research, 47(16), 8521-8536.
Hernández-Tamayo, Rogelio; Oviedo-Bocanegra, Luis M.; Fritz, Georg & Graumann, Peter L.
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Two-step chromosome segregation in the stalked budding bacterium Hyphomonas neptunium. Nature Communications, 10(1).
Jung, Alexandra; Raßbach, Anne; Pulpetta, Revathi L.; van Teeseling Muriel, C. F.; Heinrich, Kristina; Sobetzko, Patrick; Serrania, Javier; Becker, Anke & Thanbichler, Martin
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An ATP-dependent partner switch links flagellar C-ring assembly with gene expression. Proceedings of the National Academy of Sciences, 117(34), 20826-20835.
Blagotinsek, Vitan; Schwan, Meike; Steinchen, Wieland; Mrusek, Devid; Hook, John C.; Rossmann, Florian; Freibert, Sven A.; Kratzat, Hanna; Murat, Guillaume; Kressler, Dieter; Beckmann, Roland; Beeby, Morgan; Thormann, Kai M. & Bange, Gert
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Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum. Nature Communications, 11(1).
Böhm, Kati; Giacomelli, Giacomo; Schmidt, Andreas; Imhof, Axel; Koszul, Romain; Marbouty, Martial & Bramkamp, Marc
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Chromosome Segregation in Bacillus subtilis Follows an Overall Pattern of Linear Movement and Is Highly Robust against Cell Cycle Perturbations. mSphere, 5(3).
El Najjar, Nina; Geisel, David; Schmidt, Felix; Dersch, Simon; Mayer, Benjamin; Hartmann, Raimo; Eckhardt, Bruno; Lenz, Peter & Graumann, Peter L.
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Local Self-Enhancement of MinD Membrane Binding in Min Protein Pattern Formation. Journal of Molecular Biology, 432(10), 3191-3204.
Heermann, Tamara; Ramm, Beatrice; Glaser, Samson & Schwille, Petra
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Molecular architecture of the DNA-binding sites of the P-loop ATPases MipZ and ParA from Caulobacter crescentus. Nucleic Acids Research, 48(9), 4769-4779.
Corrales-Guerrero, Laura; He, Binbin; Refes, Yacine; Panis, Gaël; Bange, Gert; Viollier, Patrick H.; Steinchen, Wieland & Thanbichler, Martin
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Protein-protein interaction network controlling establishment and maintenance of switchable cell polarity. PLOS Genetics, 16(6), e1008877.
Carreira, Luís António Menezes; Tostevin, Filipe; Gerland, Ulrich & Søgaard-Andersen, Lotte
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RNA-mediated control of cell shape modulates antibiotic resistance in Vibrio cholerae. Nature Communications, 11(1).
Peschek, Nikolai; Herzog, Roman; Singh, Praveen K.; Sprenger, Marcel; Meyer, Fabian; Fröhlich, Kathrin S.; Schröger, Luise; Bramkamp, Marc; Drescher, Knut & Papenfort, Kai
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SMC and the bactofilin/PadC scaffold have distinct yet redundant functions in chromosome segregation and organization in Myxococcus xanthus. Molecular Microbiology, 114(5), 839-856.
Anand, Deepak; Schumacher, Dominik & Søgaard‐Andersen, Lotte
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Tol-Pal System and Rgs Proteins Interact to Promote Unipolar Growth and Cell Division in Sinorhizobium meliloti. mBio, 11(3).
Krol, Elizaveta; Yau, Hamish C. L.; Lechner, Marcus; Schäper, Simon; Bange, Gert; Vollmer, Waldemar & Becker, Anke
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A diffusiophoretic mechanism for ATP-driven transport without motor proteins. Nature Physics, 17(7), 850-858.
Ramm, Beatrice; Goychuk, Andriy; Khmelinskaia, Alena; Blumhardt, Philipp; Eto, Hiromune; Ganzinger, Kristina A.; Frey, Erwin & Schwille, Petra
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Dynamics of Bacterial Signal Recognition Particle at a Single Molecule Level. Frontiers in Microbiology, 12.
Mayer, Benjamin; Schwan, Meike; Oviedo-Bocanegra, Luis M.; Bange, Gert; Thormann, Kai M. & Graumann, Peter L.
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Dynamics of chromosomal target search by a membrane-integrated one-component receptor. PLOS Computational Biology, 17(2), e1008680.
Martini, Linda; Brameyer, Sophie; Hoyer, Elisabeth; Jung, Kirsten & Gerland, Ulrich
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Dynamics of the Bacillus subtilis Min System. mBio, 12(2).
Feddersen, Helge; Würthner, Laeschkir; Frey, Erwin & Bramkamp, Marc
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Four different mechanisms for switching cell polarity. PLOS Computational Biology, 17(1), e1008587.
Tostevin, Filipe; Wigbers, Manon; Søgaard-Andersen, Lotte & Gerland, Ulrich
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Learning the distribution of single-cell chromosome conformations in bacteria reveals emergent order across genomic scales. Nature Communications, 12(1).
Messelink, Joris J. B.; van Teeseling Muriel, C. F.; Janssen, Jacqueline; Thanbichler, Martin & Broedersz, Chase P.
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Mass-sensitive particle tracking to elucidate the membrane-associated MinDE reaction cycle. Nature Methods, 18(10), 1239-1246.
Heermann, Tamara; Steiert, Frederik; Ramm, Beatrice; Hundt, Nikolas & Schwille, Petra
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PomX, a ParA/MinD ATPase activating protein, is a triple regulator of cell division in Myxococcus xanthus. eLife, 10.
Schumacher, Dominik; Harms, Andrea; Bergeler, Silke; Frey, Erwin & Søgaard-Andersen, Lotte
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Single molecule/particle tracking analysis program SMTracker 2.0 reveals different dynamics of proteins within the RNA degradosome complex inBacillus subtilis. Nucleic Acids Research, 49(19), e112-e112.
Oviedo-Bocanegra, Luis M.; Hinrichs, Rebecca; Rotter, DanielAndreasOrlando; Dersch, Simon & Graumann, Peter L.
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Single-cell growth inference of Corynebacterium glutamicum reveals asymptotically linear growth. eLife, 10.
Messelink, Joris JB; Meyer, Fabian; Bramkamp, Marc & Broedersz, Chase P.
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Stable inheritance of Sinorhizobium meliloti cell growth polarity requires an FtsN-like protein and an amidase. Nature Communications, 12(1).
Krol, Elizaveta; Stuckenschneider, Lisa; Kästle, Silva Joana M.; Graumann, Peter L. & Becker, Anke
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The CTPase activity of ParB determines the size and dynamics of prokaryotic DNA partition complexes. Molecular Cell, 81(19), 3992-4007.e10.
Osorio-Valeriano, Manuel; Altegoer, Florian; Das Chandan, K.; Steinchen, Wieland; Panis, Gaël; Connolley, Lara; Giacomelli, Giacomo; Feddersen, Helge; Corrales-Guerrero, Laura; Giammarinaro, Pietro I.; Hanßmann, Juri; Bramkamp, Marc; Viollier, Patrick H.; Murray, Seán; Schäfer, Lars V.; Bange, Gert & Thanbichler, Martin
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Theory of Active Intracellular Transport by DNA Relaying. Physical Review Letters, 127(13).
Hanauer, Christian; Bergeler, Silke; Frey, Erwin & Broedersz, Chase P.
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CTP-controlled liquid–liquid phase separation of ParB. Journal of Molecular Biology, 434(2), 167401.
Babl, Leon; Giacomelli, Giacomo; Ramm, Beatrice; Gelmroth, Ann-Kathrin; Bramkamp, Marc & Schwille, Petra
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Division of labor and collective functionality in Escherichia coli under acid stress. Communications Biology, 5(1).
Brameyer, Sophie; Schumacher, Kilian; Kuppermann, Sonja & Jung, Kirsten
