TY - JOUR
T1 - Bacteria push the limits of chemotactic precision to navigate dynamic chemical gradients
AU - Brumley, Douglas R.
AU - Carrara, Francesco
AU - Hein, Andrew M.
AU - Yawata, Yutaka
AU - Levin, Simon Asher
AU - Stocker, Roman
N1 - Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019
Y1 - 2019
N2 - Ephemeral aggregations of bacteria are ubiquitous in the environment, where they serve as hotbeds of metabolic activity, nutrient cycling, and horizontal gene transfer. In many cases, these regions of high bacterial concentration are thought to form when motile cells use chemotaxis to navigate to chemical hotspots. However, what governs the dynamics of bacterial aggregations is unclear. Here, we use an experimental platform to create realistic submillimeter-scale nutrient pulses with controlled nutrient concentrations. By combining experiments, mathematical theory, and agent-based simulations, we show that individual Vibrio ordalii bacteria begin chemotaxis toward hotspots of dissolved organic matter (DOM) when the magnitude of the chemical gradient rises sufficiently far above the sensory noise that is generated by stochastic encounters with chemoattractant molecules. Each DOM hotspot is surrounded by a dynamic ring of chemotaxing cells, which congregate in regions of highDOMconcentration before dispersing as DOM diffuses and gradients become too noisy for cells to respond to. We demonstrate that V. ordalii operates close to the theoretical limits on chemotactic precision. Numerical simulations of chemotactic bacteria, in which molecule counting noise is explicitly taken into account, point at a tradeoff between nutrient acquisition and the cost of chemotactic precision. More generally, our results illustrate how limits on sensory precision can be used to understand the location, spatial extent, and lifespan of bacterial behavioral responses in ecologically relevant environments.
AB - Ephemeral aggregations of bacteria are ubiquitous in the environment, where they serve as hotbeds of metabolic activity, nutrient cycling, and horizontal gene transfer. In many cases, these regions of high bacterial concentration are thought to form when motile cells use chemotaxis to navigate to chemical hotspots. However, what governs the dynamics of bacterial aggregations is unclear. Here, we use an experimental platform to create realistic submillimeter-scale nutrient pulses with controlled nutrient concentrations. By combining experiments, mathematical theory, and agent-based simulations, we show that individual Vibrio ordalii bacteria begin chemotaxis toward hotspots of dissolved organic matter (DOM) when the magnitude of the chemical gradient rises sufficiently far above the sensory noise that is generated by stochastic encounters with chemoattractant molecules. Each DOM hotspot is surrounded by a dynamic ring of chemotaxing cells, which congregate in regions of highDOMconcentration before dispersing as DOM diffuses and gradients become too noisy for cells to respond to. We demonstrate that V. ordalii operates close to the theoretical limits on chemotactic precision. Numerical simulations of chemotactic bacteria, in which molecule counting noise is explicitly taken into account, point at a tradeoff between nutrient acquisition and the cost of chemotactic precision. More generally, our results illustrate how limits on sensory precision can be used to understand the location, spatial extent, and lifespan of bacterial behavioral responses in ecologically relevant environments.
KW - Chemotaxis
KW - Microbial ecology
KW - Motility
KW - Ocean
KW - Sensing noise
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U2 - 10.1073/pnas.1816621116
DO - 10.1073/pnas.1816621116
M3 - Article
C2 - 31097577
AN - SCOPUS:85066426348
SN - 0027-8424
VL - 166
SP - 10792
EP - 10797
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 22
ER -