Physiological adaptation in flagellar architecture improves Vibrio alginolyticus chemotaxis in complex environments

Proceedings of the National Academy of Sciences, vol. 120, pp. e2301873120

Abstract

Bacteria navigate natural habitats with a wide range of mechanical properties, from the ocean to the digestive tract and soil, by rotating helical flagella like propellers. Species differ in the number, position, and shape of their flagella, but the adaptive value of these flagellar architectures is unclear. Many species traverse multiple types of environments, such as pathogens inside and outside a host. We investigate the hypothesis that flagellar architectures mediate environment-specific benefits in the marine pathogen Vibrio alginolyticus which exhibits physiological adaptation to the mechanical environment. In addition to its single polar flagellum, the bacterium produces lateral flagella in environments that differ mechanically from water. These are known to facilitate surface motility and attachment. We use high-throughput 3D bacterial tracking to quantify chemotactic performance of both flagellar architectures in three archetypes of mechanical environments relevant to the bacterium’s native habitats: water, polymer solutions, and hydrogels. We reveal that lateral flagella impede chemotaxis in water by lowering the swimming speed but improve chemotaxis in both types of complex environments. Statistical trajectory analysis reveals two distinct underlying behavioral mechanisms: In viscous solutions of the polymer PVP K90, lateral flagella increase the swimming speed. In agar hydrogels, lateral flagella improve overall chemotactic performance, despite lowering the swimming speed, by preventing trapping in pores. Our findings show that lateral flagella are multipurpose tools with a wide range of applications beyond surfaces. They implicate flagellar architecture as a mediator of environment-specific benefits and point to a rich space of bacterial navigation behaviors in complex environments.

Authors 4

1. Marianne Grognot Aachen Institute of Medical Microbiology

   Harvard University · Universitätsklinikum Aachen · Rowland Institute at Harvard · RWTH Aachen University

   Affiliation as printed

   Institute of Medical Microbiology, Rheinisch-Westfälische Technische Hochschule University Hospital Aachen, Rheinisch-Westfälische Technische Hochschule University, Aachen 52074, Germany

   Rowland Institute, Harvard University, Cambridge, MA 02142

2. Jong Woo Nam

   Harvard University · Rowland Institute at Harvard

   Affiliation as printed

   Rowland Institute, Harvard University, Cambridge, MA 02142

3. Lauren E. Elson

   Harvard University · Rowland Institute at Harvard

   Affiliation as printed

   Rowland Institute, Harvard University, Cambridge, MA 02142

4. Katja M. Taute

   Harvard University · Rowland Institute at Harvard · Ludwig-Maximilians-Universität München

   Affiliation as printed

   Biozentrum, Ludwig-Maximilians-Universität München, Martinsried 82152, Germany

   Rowland Institute, Harvard University, Cambridge, MA 02142