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

bioRxiv (Cold Spring Harbor Laboratory)

Abstract

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, despite lowering the swimming speed, lateral flagella improve overall chemotactic performance by preventing trapping in pores. Our findings show that lateral flagella are multi-purpose 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, RWTH University Hospital Aachen, RWTH University, 52074 Aachen, Germany

   Rowland Institute, Harvard University, Cambridge, MA 02142, USA

   Institute of Medical Microbiology, RWTH University Hospital Aachen, RWTH University, 5074 Aachen, Germany

   Rowland Institute, Harvard University, Cambridge, MA 0242, USA

2. Jong Woo Nam

   University of Southern California · Harvard University · Rowland Institute at Harvard

   Affiliation as printed

   Neuroscience Graduate Program, University of Southern California, Los Angeles, CA 90007, USA

   Rowland Institute, Harvard University, Cambridge, MA 02142, USA

   Rowland Institute, Harvard University, Cambridge, MA 0242, USA

3. Lauren E. Elson

   Harvard University · Washington University in St. Louis · Rowland Institute at Harvard

   Affiliation as printed

   Rowland Institute, Harvard University, Cambridge, MA 02142, USA

   Washington University School of Medicine in St. Louis, St. Louis, MO 63110, USA

   Rowland Institute, Harvard University, Cambridge, MA 0242, USA

4. Katja M. Taute corresponding

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

   Affiliation as printed

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

   Rowland Institute, Harvard University, Cambridge, MA 02142, USA

   Biozentrum, Ludwig-Maximilians-Universität München, 8212 Martinsried, Germany

   Rowland Institute, Harvard University, Cambridge, MA 0242, USA