TY - JOUR
T1 - Ion channels enable electrical communication in bacterial communities
AU - Prindle, Arthur
AU - Liu, Jintao
AU - Asally, Munehiro
AU - Ly, San
AU - Garcia-Ojalvo, Jordi
AU - Süel, Gürol M.
N1 - Funding Information:
Acknowledgements We would like to thank S. Lockless, K. Süel, R. Wollman, T. Çag˘atay and M. Elowitz for comments during the writing of the manuscript, and C. Piggott for cloning help. A.P. is a Simons Foundation Fellow of the Helen Hay Whitney Foundation. J.G.-O. is supported by the Ministerio de Economia y Competitividad (Spain) and FEDER, under project FIS2012-37655-C02-01, and by the ICREA Academia Programme. This research was funded by the National Institutes of Health, National Institute of General Medical Sciences Grant R01 GM088428 and the National Science Foundation Grant MCB-1450867 50867 (both to G.M.S.). This work was also supported by the San Diego Center for Systems Biology (NIH Grant P50 GM085764).
Publisher Copyright:
© 2015 Macmillan Publishers Limited. All rights reserved.
PY - 2015/11/5
Y1 - 2015/11/5
N2 - The study of bacterial ion channels has provided fundamental insights into the structural basis of neuronal signalling; however, the native role of ion channels in bacteria has remained elusive. Here we show that ion channels conduct long-range electrical signals within bacterial biofilm communities through spatially propagating waves of potassium. These waves result from a positive feedback loop, in which a metabolic trigger induces release of intracellular potassium, which in turn depolarizes neighbouring cells. Propagating through the biofilm, this wave of depolarization coordinates metabolic states among cells in the interior and periphery of the biofilm. Deletion of the potassium channel abolishes this response. As predicted by a mathematical model, we further show that spatial propagation can be hindered by specific genetic perturbations to potassium channel gating. Together, these results demonstrate a function for ion channels in bacterial biofilms, and provide a prokaryotic paradigm for active, long-range electrical signalling in cellular communities.
AB - The study of bacterial ion channels has provided fundamental insights into the structural basis of neuronal signalling; however, the native role of ion channels in bacteria has remained elusive. Here we show that ion channels conduct long-range electrical signals within bacterial biofilm communities through spatially propagating waves of potassium. These waves result from a positive feedback loop, in which a metabolic trigger induces release of intracellular potassium, which in turn depolarizes neighbouring cells. Propagating through the biofilm, this wave of depolarization coordinates metabolic states among cells in the interior and periphery of the biofilm. Deletion of the potassium channel abolishes this response. As predicted by a mathematical model, we further show that spatial propagation can be hindered by specific genetic perturbations to potassium channel gating. Together, these results demonstrate a function for ion channels in bacterial biofilms, and provide a prokaryotic paradigm for active, long-range electrical signalling in cellular communities.
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U2 - 10.1038/nature15709
DO - 10.1038/nature15709
M3 - Article
C2 - 26503040
AN - SCOPUS:84946221763
SN - 0028-0836
VL - 527
SP - 59
EP - 63
JO - Nature
JF - Nature
IS - 7576
ER -