Species-Independent Attraction to Biofilms through Electrical Signaling

Jacqueline Humphries; Liyang Xiong; Jintao Liu; Arthur Prindle; Fang Yuan; Heidi A. Arjes; Lev Tsimring; Gürol M. Süel

doi:10.1016/j.cell.2016.12.014

Species-Independent Attraction to Biofilms through Electrical Signaling

Jacqueline Humphries, Liyang Xiong, Jintao Liu, Arthur Prindle, Fang Yuan, Heidi A. Arjes, Lev Tsimring, Gürol M. Süel^*

^*Corresponding author for this work

Biochemistry and Molecular Genetics

Research output: Contribution to journal › Article › peer-review

226 Scopus citations

Abstract

Bacteria residing within biofilm communities can coordinate their behavior through cell-to-cell signaling. However, it remains unclear if these signals can also influence the behavior of distant cells that are not part of the community. Using a microfluidic approach, we find that potassium ion channel-mediated electrical signaling generated by a Bacillus subtilis biofilm can attract distant cells. Integration of experiments and mathematical modeling indicates that extracellular potassium emitted from the biofilm alters the membrane potential of distant cells, thereby directing their motility. This electrically mediated attraction appears to be a generic mechanism that enables cross-species interactions, as Pseudomonas aeruginosa cells also become attracted to the electrical signal released by the B. subtilis biofilm. Cells within a biofilm community can thus not only coordinate their own behavior but also influence the behavior of diverse bacteria at a distance through long-range electrical signaling.

Original language	English (US)
Pages (from-to)	200-209.e12
Journal	Cell
Volume	168
Issue number	1-2
DOIs	https://doi.org/10.1016/j.cell.2016.12.014
State	Published - Jan 12 2017

Funding

We would like to thank S. Lockless, T. Cagatay, M. Asally, K. Süel, and J. Garcia-Ojalvo for comments during the writing of the manuscript, San Ly for help with strain construction, K. Pogliano and R. Losick for providing bacterial strains, and D.Y. Lee, J. Larkin, and L. Baumgart for helpful discussions. This work was in part supported by the San Diego Center for Systems Biology (NIH P50 GM085764) and the National Science Foundation (MCB-1616755). The following grants to G.M.S. funded this work: the NIH, National Institute of General Medical Sciences (R01 GM121888), the National Science Foundation (MCB-1450867 50867), the Defense Advanced Research Projects Agency (HR0011-16-2-0035), and the Howard Hughes Medical Institute-Simons Foundation Faculty Scholars program. J.H. was supported by the UCSD Cellular and Molecular Genetics Training Program through an institutional grant from the National Institute of General Medicine (T32 GM007240). A.P. was supported by a Simons Foundation Fellowship of the Helen Hay Whitney Foundation and holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund. L.X. and L.T. were partially supported by ONR grant N00014-16-1-2093.

Keywords

bacterial communities
biofilm
electrical signaling
ion channel
long-range signaling
membrane potential
motility
multispecies
single cell trajectories
tumbling frequency

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2016.12.014

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title = "Species-Independent Attraction to Biofilms through Electrical Signaling",

abstract = "Bacteria residing within biofilm communities can coordinate their behavior through cell-to-cell signaling. However, it remains unclear if these signals can also influence the behavior of distant cells that are not part of the community. Using a microfluidic approach, we find that potassium ion channel-mediated electrical signaling generated by a Bacillus subtilis biofilm can attract distant cells. Integration of experiments and mathematical modeling indicates that extracellular potassium emitted from the biofilm alters the membrane potential of distant cells, thereby directing their motility. This electrically mediated attraction appears to be a generic mechanism that enables cross-species interactions, as Pseudomonas aeruginosa cells also become attracted to the electrical signal released by the B. subtilis biofilm. Cells within a biofilm community can thus not only coordinate their own behavior but also influence the behavior of diverse bacteria at a distance through long-range electrical signaling.",

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author = "Jacqueline Humphries and Liyang Xiong and Jintao Liu and Arthur Prindle and Fang Yuan and Arjes, {Heidi A.} and Lev Tsimring and S{\"u}el, {G{\"u}rol M.}",

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AU - Humphries, Jacqueline

AU - Xiong, Liyang

AU - Liu, Jintao

AU - Prindle, Arthur

AU - Yuan, Fang

AU - Arjes, Heidi A.

AU - Tsimring, Lev

AU - Süel, Gürol M.

PY - 2017/1/12

Y1 - 2017/1/12

N2 - Bacteria residing within biofilm communities can coordinate their behavior through cell-to-cell signaling. However, it remains unclear if these signals can also influence the behavior of distant cells that are not part of the community. Using a microfluidic approach, we find that potassium ion channel-mediated electrical signaling generated by a Bacillus subtilis biofilm can attract distant cells. Integration of experiments and mathematical modeling indicates that extracellular potassium emitted from the biofilm alters the membrane potential of distant cells, thereby directing their motility. This electrically mediated attraction appears to be a generic mechanism that enables cross-species interactions, as Pseudomonas aeruginosa cells also become attracted to the electrical signal released by the B. subtilis biofilm. Cells within a biofilm community can thus not only coordinate their own behavior but also influence the behavior of diverse bacteria at a distance through long-range electrical signaling.

AB - Bacteria residing within biofilm communities can coordinate their behavior through cell-to-cell signaling. However, it remains unclear if these signals can also influence the behavior of distant cells that are not part of the community. Using a microfluidic approach, we find that potassium ion channel-mediated electrical signaling generated by a Bacillus subtilis biofilm can attract distant cells. Integration of experiments and mathematical modeling indicates that extracellular potassium emitted from the biofilm alters the membrane potential of distant cells, thereby directing their motility. This electrically mediated attraction appears to be a generic mechanism that enables cross-species interactions, as Pseudomonas aeruginosa cells also become attracted to the electrical signal released by the B. subtilis biofilm. Cells within a biofilm community can thus not only coordinate their own behavior but also influence the behavior of diverse bacteria at a distance through long-range electrical signaling.

KW - bacterial communities

KW - biofilm

KW - electrical signaling

KW - ion channel

KW - long-range signaling

KW - membrane potential

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KW - single cell trajectories

KW - tumbling frequency

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Species-Independent Attraction to Biofilms through Electrical Signaling

Abstract

Funding

Keywords

ASJC Scopus subject areas

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