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      Multi-scale dynamic imaging reveals that cooperative motility behaviors promote efficient predation in bacteria

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          Abstract

          Many species, such as fish schools or bird flocks, rely on collective motion to forage, prey, or escape predators. Likewise, Myxococcus xanthus forages and moves collectively to prey and feed on other bacterial species. These activities require two distinct motility machines enabling adventurous (A) and social (S) gliding, however when and how these mechanisms are used has remained elusive. Here, we address this long-standing question by applying multiscale semantic cell tracking during predation. We show that: (1) foragers and swarms can comprise A- and S-motile cells, with single cells exchanging frequently between these groups; (2) A-motility is critical to ensure the directional movement of both foragers and swarms; (3) the combined action of A- and S-motile cells within swarms leads to increased predation efficiencies. These results challenge the notion that A- and S-motilities are exclusive to foragers and swarms, and show that these machines act synergistically to enhance predation efficiency.

          Abstract

          Myxococcus xanthus forages and moves collectively to prey and feed on other bacterial species. Here, the authors challenge the conventional idea that during Myxococcus xanthus predation, A- and S-motilities are limited to specific forager and swarm roles and reveal a synergistic interaction between these motilities to enhance predation efficiency.

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          Most cited references30

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          UMAP: Uniform Manifold Approximation and Projection

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            Collective motion

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              Myxobacteria: Moving, Killing, Feeding, and Surviving Together

              Myxococcus xanthus, like other myxobacteria, is a social bacterium that moves and feeds cooperatively in predatory groups. On surfaces, rod-shaped vegetative cells move in search of the prey in a coordinated manner, forming dynamic multicellular groups referred to as swarms. Within the swarms, cells interact with one another and use two separate locomotion systems. Adventurous motility, which drives the movement of individual cells, is associated with the secretion of slime that forms trails at the leading edge of the swarms. It has been proposed that cellular traffic along these trails contributes to M. xanthus social behavior via stigmergic regulation. However, most of the cells travel in groups by using social motility, which is cell contact-dependent and requires a large number of individuals. Exopolysaccharides and the retraction of type IV pili at alternate poles of the cells are the engines associated with social motility. When the swarms encounter prey, the population of M. xanthus lyses and takes up nutrients from nearby cells. This cooperative and highly density-dependent feeding behavior has the advantage that the pool of hydrolytic enzymes and other secondary metabolites secreted by the entire group is shared by the community to optimize the use of the degradation products. This multicellular behavior is especially observed in the absence of nutrients. In this condition, M. xanthus swarms have the ability to organize the gliding movements of 1000s of rods, synchronizing rippling waves of oscillating cells, to form macroscopic fruiting bodies, with three subpopulations of cells showing division of labor. A small fraction of cells either develop into resistant myxospores or remain as peripheral rods, while the majority of cells die, probably to provide nutrients to allow aggregation and spore differentiation. Sporulation within multicellular fruiting bodies has the benefit of enabling survival in hostile environments, and increases germination and growth rates when cells encounter favorable conditions. Herein, we review how these social bacteria cooperate and review the main cell–cell signaling systems used for communication to maintain multicellularity.
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                Author and article information

                Contributors
                antoine.legall@cbs.cnrs.fr
                nollmann@cbs.cnrs.fr
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                11 September 2023
                11 September 2023
                2023
                : 14
                : 5588
                Affiliations
                [1 ]GRID grid.121334.6, ISNI 0000 0001 2097 0141, Centre de Biologie Structurale, CNRS UMR 5048, INSERM U1054, Université de Montpellier, ; 60 rue de Navacelles, 34090 Montpellier, France
                [2 ]GRID grid.469471.9, ISNI 0000 0004 0369 4095, Laboratoire de Chimie Bactérienne, ; Marseille, France
                Author information
                http://orcid.org/0009-0001-9983-9943
                http://orcid.org/0000-0003-3339-2349
                Article
                41193
                10.1038/s41467-023-41193-x
                10495355
                37696789
                cd101cd2-f48f-4ec7-bc79-6c1d36bc7050
                © Springer Nature Limited 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 9 December 2022
                : 21 August 2023
                Funding
                Funded by: FundRef https://doi.org/10.13039/100010663, EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council);
                Award ID: JAWS
                Award ID: Episcope
                Award Recipient :
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                © Springer Nature Limited 2023

                Uncategorized
                cellular imaging,motility,bacteriology
                Uncategorized
                cellular imaging, motility, bacteriology

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