[en] Spatiotemporal organization of individuals within growing bacterial colonies is a key determinant of intraspecific interactions and colony-scale heterogeneities. The evolving cellular distribution, in relation to the genealogical lineage, is thus central to our understanding of bacterial fate across scales. Yet, how bacteria self-organize genealogically as a colony expands has remained unknown. Here, by developing a custom-built label-free algorithm, we track and study the genesis and evolution of emergent self-similar genealogical enclaves, whose dynamics are governed by biological activity. Topological defects at enclave boundaries tune finger-like morphologies of the active interfaces. The Shannon entropy of cell arrangements reduce over time; with faster-dividing cells possessing higher spatial affinity to genealogical relatives, at the cost of a well-mixed, entropically favorable state. Our coarse-grained lattice model demonstrates that genealogical enclaves emerge due to an interplay of division-mediated dispersal, stochasticity of division events, and cell-cell interactions. The study reports so-far hidden emergent self-organizing features arising due to entropic suppression, ultimately modulating intraspecific genealogical distances within bacterial colonies.
Disciplines :
Physical, chemical, mathematical & earth Sciences: Multidisciplinary, general & others
Author, co-author :
RANI, Garima ; University of Luxembourg > Faculty of Science, Technology and Medicine > Department of Physics and Materials Science > Team Anupam SENGUPTA
FNR11572821 - MBRACE - Biophysics Of Microbial Adaptation To Fluctuations In The Environment, 2017 (15/05/2018-14/11/2024) - Anupam Sengupta FNR13719464 - TOPOFLUME - Topological Fluid Mechanics: Decoding Emergent Dynamics In Anisotropic Fluids And Living Systems, 2019 (01/09/2020-31/08/2023) - Anupam Sengupta
Name of the research project :
R-AGR-3401 - A17/MS/11572821/MBRACE - part UL - SENGUPTA Anupam R-AGR-3692 - C19/MS/13719464/TOPOFLUME - SENGUPTA Anupam U-AGR-8060 - HFSP Postdoctoral Fellowship G. Rani - p - SENGUPTA Anupam U-AGR-6003 - IAS-AUDACITY CAMEOS - SENGUPTA Anupam
Funders :
University of Luxembourg Human Frontier Science Program FNR
Funding text :
We gratefully acknowledge the support from the Institute for Advanced Studies, University of Luxembourg (AUDACITY grant: IAS-20/CAMEOS to A.S.) and a Human Frontier Science Program Cross Disciplinary Fellowship ( LT 00230/2021-C to G.R.). We thank J. Nguyen for the raw image displayed in Fig. S6 A. A.S. thanks Luxembourg National Research Fund for the ATTRACT Investigator Grant ( A17/MS/ 11572821/MBRACE ) and a CORE Grant ( C19/MS/13719464/TOPOFLUME/Sengupta ) for supporting this work.
Davey, M.E., O'toole, G.A., Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev., 64, 2000, 847.
Jovel, J., Dieleman, L.A., et al., Wine, E., Nagarajan, M., (eds.) Metagenomics, 2018, Academic Press, 197–213.
Waters, C.M., Bassler, B.L., QUORUM SENSING: Cell-to-Cell Communication in Bacteria. Annu. Rev. Cell Dev. Biol. 21 (2005), 319–346.
Prindle, A., Liu, J., et al., Süel, G.M., Ion channels enable electrical communication in bacterial communities. Nature 527 (2015), 59–63.
Liu, J., Prindle, A., et al., Süel, G.M., Metabolic co-dependence gives rise to collective oscillations within biofilms. Nature 523 (2015), 550–554.
Fridman, O., Goldberg, A., et al., Balaban, N.Q., Optimization of lag time underlies antibiotic tolerance in evolved bacterial populations. Nature 513 (2014), 418–421.
Dhar, J., Thai, A.L.P., et al., Sengupta, A., Self-regulation of phenotypic noise synchronizes emergent organization and active transport in confluent microbial environments. Nat. Phys. 18 (2022), 945–951.
Wittmann, R., Nguyen, G.H., et al., Sengupta, A., Collective mechano-response dynamically tunes cell-size distributions in growing bacterial colonies. Commun. Phys., 6, 2023, 331.
Nadell, C.D., Drescher, K., Foster, K.R., Spatial structure, cooperation and competition in biofilms. Nat. Rev. Microbiol. 14 (2016), 589–600.
Dal Co, A., Ackermann, M., van Vliet, S., Spatial self-organization of metabolism in microbial systems: A matter of enzymes and chemicals. Cell. Syst. 14 (2023), 98–108.
Kim, D., Barraza, J.P., et al., Koo, H., Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries. Proc. Natl. Acad. Sci. USA 117 (2020), 12375–12386.
You, Z., Pearce, D.J.G., et al., Giomi, L., Geometry and Mechanics of Microdomains in Growing Bacterial Colonies. Phys. Rev. X, 8, 2018, 031065.
Dell'Arciprete, D., Blow, M.L., et al., Poon, W.C.K., A growing bacterial colony in two dimensions as an active nematic. Nat. Commun., 9, 2018, 4190.
Los, R., et al. Defect dynamics in growing bacterial colonies. Preprint at arXiv, 2022, 10.48550/arXiv.2003.10509.
Tan, J., Zuniga, C., Zengler, K., Unraveling interactions in microbial communities - from co-cultures to microbiomes. J. Microbiol. 53 (2015), 295–305.
Dal Co, A., van Vliet, S., et al., Ackermann, M., Short-range interactions govern the dynamics and functions of microbial communities. Nat. Ecol. Evol. 4 (2020), 366–375.
Schneider, A.F.L., Hackenberger, C.P.R., Fluorescent labelling in living cells. Curr. Opin. Biotechnol. 48 (2017), 61–68.
Hallatschek, O., Hersen, P., et al., Nelson, D.R., Genetic drift at expanding frontiers promotes gene segregation. Proc. Natl. Acad. Sci. USA, 104, 2007, 19926.
Bottery, M.J., Passaris, I., et al., van der Woude, M.W., Spatial Organization of Expanding Bacterial Colonies Is Affected by Contact-Dependent Growth Inhibition. Curr. Biol. 29 (2019), 3622–3634.e5.
Berg, S., Kutra, D., et al., Kreshuk, A., ilastik: interactive machine learning for (bio)image analysis. Nat. Methods 16 (2019), 1226–1232.
Young, J., Elowitz, M., CaltechDATA. 2021.
Stylianidou, S., Brennan, C., et al., Wiggins, P.A., SuperSegger: robust image segmentation, analysis and lineage tracking of bacterial cells. Mol. Microbiol. 102 (2016), 690–700.
Ollion, J., Maliet, M., et al., Deforet, M., DiSTNet2D: Leveraging Long-Range Temporal Information for Efficient Segmentation and Tracking. PRX Life, 2, 2024, 023004.
You, Z., Pearce, D.J.G., et al., Giomi, L., Mono- to Multilayer Transition in Growing Bacterial Colonies. Phys. Rev. Lett., 123, 2019, 178001.
Marín, D., Martín, M., Sabater, B., Entropy decrease associated to solute compartmentalization in the cell. Biosystems, 98, 2009, 31.
Popovic, M., Entropy change of open thermodynamic systems in self-organizing processes. Therm. Sci. 18 (2014), 1425–1432.
Schrödinger, E., Penrose, R., What is Life?: With Mind and Matter and Autobiographical Sketches, Canto. 1992, Cambridge University Press.
Vranken, I., Baudry, J., et al., Bogaert, J., A review on the use of entropy in landscape ecology: heterogeneity, unpredictability, scale dependence and their links with thermodynamics. Landsc. Ecol. 30 (2015), 51–65.
Chaikin, P.M., Lubensky, T.C., Principles of Condensed Matter Physics. 1995, Cambridge University Press.
Zhang, D.-Q., Chen, P.-C., et al., Li, B., Topological defect-mediated morphodynamics of active-active interfaces. Proc. Natl. Acad. Sci. USA, 119, 2022, e2122494119.
Doostmohammadi, A., Thampi, S.P., Yeomans, J.M., Defect-Mediated Morphologies in Growing Cell Colonies. Phys. Rev. Lett., 117, 2016, 048102.
Rodríguez-Franco, P., Brugués, A., et al. Long-lived force patterns and deformation waves at repulsive epithelial boundaries. Nat. Mater. 16 (2017), 1029–1037.
Giomi, L., Geometry and Topology of Turbulence in Active Nematics. Phys. Rev. X, 5, 2015, 031003.
Ginovart, M., López, D., et al., Silbert, M., ▪▪▪. Phys. Stat. Mech. Appl., 305, 2002, 604.
Stoop, R.L., Tierno, P., Clogging and jamming of colloidal monolayers driven across disordered landscapes. Commun. Phys., 1, 2018, 68.
Delarue, M., Hartung, J., et al., Hallatschek, O., Self-driven jamming in growing microbial populations. Nat. Phys. 12 (2016), 762–766.
Bray, A., Theory of phase-ordering kinetics. Adv. Phys. 43 (1994), 357–459.
de Gennes, P.G., Scaling Concepts in Polymer Physics. 1979.
Flory, P.J., Principles Of Polymer Chemistry. 1953, Cornell University Press, New York.
Limoli, D.H., Jones, C.J., Wozniak, D.J., Bacterial Extracellular Polysaccharides in Biofilm Formation and Function. Microbiology Spectrum, 3, 2015, ▪▪▪, 10.1128/microbiolspec.mb.
Sauer, K., Stoodley, P., et al., Bjarnsholt, T., The biofilm life cycle: expanding the conceptual model of biofilm formation. Nat. Rev. Microbiol. 20 (2022), 608–620.
Kan, A., Del Valle, I., et al., Haseloff, J., Intercellular adhesion promotes clonal mixing in growing bacterial populations. J. R. Soc. Interface, 15, 2018, 20180406.
Gralka, M., Stiewe, F., et al., Hallatschek, O., Allele surfing promotes microbial adaptation from standing variation. Ecol. Lett. 19 (2016), 889–898.
Farrell, F.D., Gralka, M., et al., Waclaw, B., Mechanical interactions in bacterial colonies and the surfing probability of beneficial mutations. J. R. Soc. Interface, 14, 2017, 20170073.
Kennard, A.S., et al. ▪▪▪. Phys. Rev. E, 93, 2016, 012408.
Bhaskar, K.R., Garik, P., et al., LaMont, J.T., Viscous fingering of HCI through gastric mucin. Nature 360 (1992), 458–461.
Marmottant, P., Mgharbel, A., et al., Delanoë-Ayari, H., The role of fluctuations and stress on the effective viscosity of cell aggregates. Proc. Natl. Acad. Sci. USA 106 (2009), 17271–17275.
Jauffred, L., Munk Vejborg, R., et al., Oddershede, L.B., Chirality in microbial biofilms is mediated by close interactions between the cell surface and the substratum. ISME J. 11 (2017), 1688–1701.
Lozupone, C.A., Stombaugh, J.I., et al., Knight, R., Diversity, stability and resilience of the human gut microbiota. Nature 489 (2012), 220–230.
Chen, W.-P., et al. Composition Analysis and Feature Selection of the Oral Microbiota Associated with Periodontal Disease. BioMed Res. Int., 2018, 2018, 3130607.
Schindelin, J., Arganda-Carreras, I., et al., Cardona, A., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
Mary, H., Brouhard, G., Kappa (κ): Analysis of Curvature in Biological Image Data using B-splines. Preprint at bioRxiv, 2019, 10.1101/852772.
Huterer, D., Vachaspati, T., Distribution of singularities in the cosmic microwave background polarization. Phys. Rev. D, 72, 2005, 043004.