Encoding Membrane-Potential-Based Memory within a Microbial Community

Chih Yu Yang, Maja Bialecka-Fornal, Colleen Weatherwax, Joseph W. Larkin, Arthur Prindle, Jintao Liu, Jordi Garcia-Ojalvo, Gürol M. Süel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

81 Scopus citations

Abstract

Cellular membrane potential plays a key role in the formation and retrieval of memories in the metazoan brain, but it remains unclear whether such memory can also be encoded in simpler organisms like bacteria. Here, we show that single-cell-level memory patterns can be imprinted in bacterial biofilms by light-induced changes in the membrane potential. We demonstrate that transient optical perturbations generate a persistent and robust potassium-channel-mediated change in the membrane potential of bacteria within the biofilm. The light-exposed cells respond in an anti-phase manner, relative to unexposed cells, to both natural and induced oscillations in extracellular ion concentrations. This anti-phase response, which persists for hours following the transient optical stimulus, enables a direct single-cell resolution visualization of spatial memory patterns within the biofilm. The ability to encode robust and persistent membrane-potential-based memory patterns could enable computations within prokaryotic communities and suggests a parallel between neurons and bacteria.

Original languageEnglish (US)
Pages (from-to)417-423.e3
JournalCell Systems
Volume10
Issue number5
DOIs
StatePublished - May 20 2020

Funding

We thank Leticia Galera-Laporta, Dong-yeon D. Lee, and Kaito Kikuchi for useful discussions; G.M.S. acknowledges support for this research from the National Institute of General Medical Sciences (grant R01 GM121888 to G.M.S.) and the Howard Hughes Medical Institute-Simons Foundation Faculty Scholars program. J.G.-O. acknowledges support from the Spanish Ministry of Science, Innovation and Universities and FEDER (project PGC2018-101251-B-I00 and “' Maria de Maeztu ” Programme for Units of Excellence in R\&D, grant CEX2018-000792-M) , and from the Generalitat de Catalunya (ICREA Academia programme). We thank Leticia Galera-Laporta, Dong-yeon D. Lee, and Kaito Kikuchi for useful discussions; G.M.S. acknowledges support for this research from the National Institute of General Medical Sciences (grant R01 GM121888 to G.M.S.) and the Howard Hughes Medical Institute-Simons Foundation Faculty Scholars program. J.G.-O. acknowledges support from the Spanish Ministry of Science, Innovation and Universities and FEDER (project PGC2018-101251-B-I00 and ?'Maria de Maeztu? Programme for Units of Excellence in R\&D, grant CEX2018-000792-M), and from the Generalitat de Catalunya (ICREA Academia programme). G.M.S. M.B.-F. C.-Y.Y. A.P. J.L. and J.G.-O. designed the research. M.B.-F. C.-Y.Y. A.P. and J.L. performed the experiments. G.M.S. C.W. and J.G.-O. performed the mathematical modeling. M.B.-F, C.-Y.Y. C.W. and J.W.L. performed the data analysis. G.M.S. M.B.-F. C.-Y.Y. C.W. and J.G.-O. wrote the manuscript. All authors discussed the manuscript. The authors declare no competing interests.

Keywords

  • Hodgkin-Huxley
  • anti-phase
  • biofilm
  • ion channels
  • membrane potential
  • memory
  • microbial communities
  • optical
  • persistent
  • robust

ASJC Scopus subject areas

  • Pathology and Forensic Medicine
  • Histology
  • Cell Biology

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