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      Speed-dependent chemotactic precision in marine bacteria

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          Significance

          Our understanding of bacterial chemotaxis, a fundamental nutrient-seeking strategy in the microbial world, mainly derives from Escherichia coli. However, it has become clear that marine bacteria evolved fundamentally different chemotaxis adaptations, often allowing them to accumulate at resource peaks more tightly and rapidly than E. coli. We studied the origin of this high chemotactic precision and found that it lies in an unexpected dependence of chemotaxis on swimming speed: faster cells have substantially higher precision, counter to all known models of chemotaxis. We elucidate this finding through a combination of single-cell tracking of thousands of marine bacteria in microfluidic gradients and a mathematical model of chemotaxis that explicitly accounts for swimming speed in the chemotaxis pathway.

          Abstract

          Chemotaxis underpins important ecological processes in marine bacteria, from the association with primary producers to the colonization of particles and hosts. Marine bacteria often swim with a single flagellum at high speeds, alternating “runs” with either 180° reversals or ∼90° “flicks,” the latter resulting from a buckling instability of the flagellum. These adaptations diverge from Escherichia coli’s classic run-and-tumble motility, yet how they relate to the strong and rapid chemotaxis characteristic of marine bacteria has remained unknown. We investigated the relationship between swimming speed, run–reverse–flick motility, and high-performance chemotaxis by tracking thousands of Vibrio alginolyticus cells in microfluidic gradients. At odds with current chemotaxis models, we found that chemotactic precision—the strength of accumulation of cells at the peak of a gradient—is swimming-speed dependent in V. alginolyticus. Faster cells accumulate twofold more tightly by chemotaxis compared with slower cells, attaining an advantage in the exploitation of a resource additional to that of faster gradient climbing. Trajectory analysis and an agent-based mathematical model revealed that this unexpected advantage originates from a speed dependence of reorientation frequency and flicking, which were higher for faster cells, and was compounded by chemokinesis, an increase in speed with resource concentration. The absence of any one of these adaptations led to a 65–70% reduction in the population-level resource exposure. These findings indicate that, contrary to what occurs in E. coli, swimming speed can be a fundamental determinant of the gradient-seeking capabilities of marine bacteria, and suggest a new model of bacterial chemotaxis.

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          Author and article information

          Journal
          Proc Natl Acad Sci U S A
          Proc. Natl. Acad. Sci. U.S.A
          pnas
          pnas
          PNAS
          Proceedings of the National Academy of Sciences of the United States of America
          National Academy of Sciences
          0027-8424
          1091-6490
          2 August 2016
          20 July 2016
          : 113
          : 31
          : 8624-8629
          Affiliations
          [1] aDepartment of Mechanical Engineering, Massachusetts Institute of Technology , Cambridge, MA 02139;
          [2] bDepartment of Civil and Environmental Engineering, Massachusetts Institute of Technology , Cambridge, MA 02139;
          [3] cInstitute for Bioengineering, The University of Edinburgh , Edinburgh EH9 3DW, United Kingdom;
          [4] dCentre for Synthetic and Systems Biology, The University of Edinburgh , Edinburgh EH9 3BF, United Kingdom;
          [5] e Institute for Environmental Engineering , Department of Civil, Environmental and Geomatic Engineering, Eidgenössische Technische Hochschule (ETH) Zürich, 8093 Zurich, Switzerland
          Author notes
          1To whom correspondence may be addressed. Email: kwangms@ 123456mit.edu or romanstocker@ 123456ethz.ch .

          Edited by Victor Sourjik, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany, and accepted by Editorial Board Member Herbert Levine June 10, 2016 (received for review February 10, 2016)

          Author contributions: K.S., F.M., and R.S. designed research; K.S. performed research; K.S. and F.M. contributed new reagents/analytic tools; K.S. analyzed data; and K.S., F.M., and R.S. wrote the paper.

          Article
          PMC4978249 PMC4978249 4978249 201602307
          10.1073/pnas.1602307113
          4978249
          27439872
          bc6539da-452a-4cc4-9541-7180d11c2148
          History
          Page count
          Pages: 6
          Funding
          Funded by: HHS | National Institutes of Health (NIH) 100000002
          Award ID: 1R01GM100473
          Funded by: Gordon and Betty Moore Foundation 100000936
          Award ID: award 3783
          Categories
          Physical Sciences
          Environmental Sciences
          Biological Sciences
          Biophysics and Computational Biology

          motility,chemotaxis,run–reverse–flick,ocean,chemokinesis

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