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A multiscale 3D chemotaxis assay reveals bacterial navigation mechanisms.

ABSTRACT: How motile bacteria navigate environmental chemical gradients has implications ranging from health to climate science, but the underlying behavioral mechanisms are unknown for most species. The well-studied navigation strategy of Escherichia coli forms a powerful paradigm that is widely assumed to translate to other bacterial species. This assumption is rarely tested because of a lack of techniques capable of bridging scales from individual navigation behavior to the resulting population-level chemotactic performance. Here, we present such a multiscale 3D chemotaxis assay by combining high-throughput 3D bacterial tracking with microfluidically created chemical gradients. Large datasets of 3D trajectories yield the statistical power required to assess chemotactic performance at the population level, while simultaneously resolving the underlying 3D navigation behavior for every individual. We demonstrate that surface effects confound typical 2D chemotaxis assays, and reveal that, contrary to previous reports, Caulobacter crescentus breaks with the E. coli paradigm.

SUBMITTER: Grognot M

PROVIDER: S-EPMC8175578 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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A multiscale 3D chemotaxis assay reveals bacterial navigation mechanisms.

Grognot Marianne M Taute Katja M KM

Communications biology 20210603 1

How motile bacteria navigate environmental chemical gradients has implications ranging from health to climate science, but the underlying behavioral mechanisms are unknown for most species. The well-studied navigation strategy of Escherichia coli forms a powerful paradigm that is widely assumed to translate to other bacterial species. This assumption is rarely tested because of a lack of techniques capable of bridging scales from individual navigation behavior to the resulting population-level c ...[more]

PMID: 34083715

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Project description:Considering the essential role of chemotaxis of adherent, slow-moving cells in processes such as tumor metastasis or wound healing, a detailed understanding of the mechanisms and cues that direct migration of cells through tissues is highly desirable. The state-of-the-art chemotaxis instruments (e.g. microfluidic-based devices, bridge assays) can generate well-defined, long-term stable chemical gradients, crucial for quantitative investigation of chemotaxis in slow-moving cells. However, the majority of chemotaxis tools are designed for the purpose of an in-depth, but labor-intensive analysis of migratory behavior of single cells. This is rather inefficient for applications requiring higher experimental throughput, as it is the case of e.g. clinical examinations, chemoattractant screening or studies of the chemotaxis-related signaling pathways based on subcellular perturbations. Here, we present an advanced migration assay for accelerated and facilitated evaluation of the chemotactic response of slow-moving cells. The revised chemotaxis chamber contains a hydrogel microstructure-the migration arena, designed to enable identification of chemotactic behavior of a cell population in respect to the end-point of the experiment. At the same time, the assay in form of a microscopy slide enables direct visualization of the cells in either 2D or 3D environment, and provides a stable and linear gradient of chemoattractant. We demonstrate the correctness of the assay on the model study of HT-1080 chemotaxis in 3D and on 2D surface. Finally, we apply the migration arena chemotaxis assay to screen for a chemoattractant of primary keratinocytes, cells that play a major role in wound healing, being responsible for skin re-epithelialization and a successful wound closure. In direction of new therapeutic strategies to promote wound repair, we identified the chemotactic activity of the epithelial growth factor receptor (EGFR) ligands EGF and TGFα (transforming growth factor α).

Dataset Information

A multiscale 3D chemotaxis assay reveals bacterial navigation mechanisms.

Publications

A multiscale 3D chemotaxis assay reveals bacterial navigation mechanisms.

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