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Novel form of collective movement by soil bacteria

Abstract

Although migrations are essential for soil microorganisms to exploit scarce and heterogeneously distributed resources, bacterial mobility in soil remains poorly studied due to experimental limitations. In this study, time-lapse images collected using live microscopy techniques captured collective and coordinated groups of B. subtilis cells exhibiting “crowd movement”. Groups of B. subtilis cells moved through transparent soil (nafion polymer with particle size resembling sand) toward plant roots and re-arranged dynamically around root tips in the form of elongating and retracting “flocks” resembling collective behaviour usually associated with higher organisms (e.g., bird flocks or fish schools). Genetic analysis reveals B. subtilis flocks are likely driven by the diffusion of extracellular signalling molecules (e.g., chemotaxis, quorum sensing) and may be impacted by the physical obstacles and hydrodynamics encountered in the soil like environment. Our findings advance understanding of bacterial migration through soil matrices and expand known behaviours for coordinated bacterial movement.

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Fig. 1: Crowd movement.
Fig. 2: Crowd motility may be a mechanism to enhance colonization of the host.
Fig. 3: Morpho-dynamics of bacterial flock.
Fig. 4: Crowd movement emerges from biophysical interactions in pore space.
Fig. 5: A complex combination of genes is involved in flock formation.
Fig. 6: Model indicates the strength of cell-to-cell communication is critical to coordinate movement towards the host.

Data availability

The link https://zenodo.org/record/4946262 provides the codes for numerical simulations of models of bacterial crowd movements. Processed image data and code for analysis of bacterial flocks is available at: https://github.com/LionelDupuy/CrowdMovement.

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Acknowledgements

The James Hutton Institute & Scotland’s Rural College were supported by funds from the Rural and Environment Science and Analytical Services Division of the Scottish Government. We thank Margarita Kalamara, Adam Ostrowski and the NSW laboratory for sharing their strains with us, Elliot Erskine, Jacqueline Marshall from JHI James Hutton Institute for advice on B. subtilis culture and other laboratory requirements, and Kathryn Wright from the James Hutton Institute for help with confocal microscopy. This work was funded by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Grant agreement No. 647857-SENSOILS). We also acknowledge the funding from the Spanish Ministry of Science and Innovation (MICINN) under de project MICROCROWD (PID2020-112950RR-I00). Work in the NSW laboratory is funded by the Biotechnology and Biological Science Research Council (BBSRC) [BB/P001335/1, BB/R012415/1].

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Funding Acquisition: LD. Conceptualisation: LXD, TJD, NH, IE. Experimental Work: IE, DP, YL, GHM, TS. Data Analysis: IE, LD, MM. Mathematical Modelling: MM, MP, LXD. Supervision: TSG, MM, MP, NRS-W, NH, TJD, LXD. Validation: LE, MK, NSW, FAD. Visualisation: LE, MK. Writing – original draft: IE, LXD. Writing – review & editing: MM, TSG, MM, MP, NRS-W, NH, TJD, LXD.

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Correspondence to L. X. Dupuy.

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Engelhardt, I.C., Patko, D., Liu, Y. et al. Novel form of collective movement by soil bacteria. ISME J 16, 2337–2347 (2022). https://doi.org/10.1038/s41396-022-01277-w

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