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

Journal: Cell systems 2021;10(5):417-423.e3

PMID: 32343961

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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.

Address: Division of Biological Sciences, University of California, San Diego, Pacific Hall Room 2225B, Mail Code 0347, 9500 Gilman Drive, La Jolla, CA 92093, USA.; Division of Biological Sciences, University of California, San Diego, Pacific Hall Room 2225B, Mail Code 0347, 9500 Gilman Drive, La Jolla, CA 92093, USA; Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, IL 60611, USA.; Division of Biological Sciences, University of California, San Diego, Pacific Hall Room 2225B, Mail Code 0347, 9500 Gilman Drive, La Jolla, CA 92093, USA; Center for Infectious Diseases Research and Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing 100084, People's Republic of China.; Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona Biomedical Research Park, Barcelona 08003, Spain.; Division of Biological Sciences, University of California, San Diego, Pacific Hall Room 2225B, Mail Code 0347, 9500 Gilman Drive, La Jolla, CA 92093, USA; San Diego Center for Systems Biology, University of California, San Diego, La Jolla, CA 92093, USA; Center for Microbiome Innovation, University of California, San Diego, La Jolla, CA 92093-0380, USA. Electronic address: [email protected].

DOI: 10.1016/j.cels.2020.04.002

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MeSH Terms: Bacteria, Biofilms, Membrane Potentials, Memory, Microbiota, Models, Theoretical, Optical Phenomena, Potassium Channels, Voltage-Sensitive Dye Imaging