Literature DB >> 32343961

Encoding Membrane-Potential-Based Memory within a Microbial Community.

Chih-Yu Yang1, Maja Bialecka-Fornal1, Colleen Weatherwax1, Joseph W Larkin1, Arthur Prindle2, Jintao Liu3, Jordi Garcia-Ojalvo4, Gürol M Süel5.   

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.
Copyright © 2020 Elsevier Inc. All rights reserved.

Entities:  

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

Year:  2020        PMID: 32343961      PMCID: PMC7286314          DOI: 10.1016/j.cels.2020.04.002

Source DB:  PubMed          Journal:  Cell Syst        ISSN: 2405-4712            Impact factor:   10.304


  23 in total

1.  Rational design of memory in eukaryotic cells.

Authors:  Caroline M Ajo-Franklin; David A Drubin; Julian A Eskin; Elaine P S Gee; Dirk Landgraf; Ira Phillips; Pamela A Silver
Journal:  Genes Dev       Date:  2007-09-15       Impact factor: 11.361

2.  Very long-term memories may be stored in the pattern of holes in the perineuronal net.

Authors:  Roger Y Tsien
Journal:  Proc Natl Acad Sci U S A       Date:  2013-07-05       Impact factor: 11.205

3.  Voltage-gated calcium flux mediates Escherichia coli mechanosensation.

Authors:  Giancarlo N Bruni; R Andrew Weekley; Benjamin J T Dodd; Joel M Kralj
Journal:  Proc Natl Acad Sci U S A       Date:  2017-08-14       Impact factor: 11.205

4.  Fiji: an open-source platform for biological-image analysis.

Authors:  Johannes Schindelin; Ignacio Arganda-Carreras; Erwin Frise; Verena Kaynig; Mark Longair; Tobias Pietzsch; Stephan Preibisch; Curtis Rueden; Stephan Saalfeld; Benjamin Schmid; Jean-Yves Tinevez; Daniel James White; Volker Hartenstein; Kevin Eliceiri; Pavel Tomancak; Albert Cardona
Journal:  Nat Methods       Date:  2012-06-28       Impact factor: 28.547

5.  Improved memory devices for synthetic cells.

Authors:  Joanne M L Ho; Matthew R Bennett
Journal:  Science       Date:  2018-04-13       Impact factor: 47.728

6.  Signal Percolation within a Bacterial Community.

Authors:  Joseph W Larkin; Xiaoling Zhai; Kaito Kikuchi; Samuel E Redford; Arthur Prindle; Jintao Liu; Sacha Greenfield; Aleksandra M Walczak; Jordi Garcia-Ojalvo; Andrew Mugler; Gürol M Süel
Journal:  Cell Syst       Date:  2018-07-25       Impact factor: 10.304

7.  Metabolic basis of brain-like electrical signalling in bacterial communities.

Authors:  Rosa Martinez-Corral; Jintao Liu; Arthur Prindle; Gürol M Süel; Jordi Garcia-Ojalvo
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-06-10       Impact factor: 6.237

8.  Channelrhodopsin-2, a directly light-gated cation-selective membrane channel.

Authors:  Georg Nagel; Tanjef Szellas; Wolfram Huhn; Suneel Kateriya; Nona Adeishvili; Peter Berthold; Doris Ollig; Peter Hegemann; Ernst Bamberg
Journal:  Proc Natl Acad Sci U S A       Date:  2003-11-13       Impact factor: 11.205

9.  Metabolic co-dependence gives rise to collective oscillations within biofilms.

Authors:  Jintao Liu; Arthur Prindle; Jacqueline Humphries; Marçal Gabalda-Sagarra; Munehiro Asally; Dong-yeon D Lee; San Ly; Jordi Garcia-Ojalvo; Gürol M Süel
Journal:  Nature       Date:  2015-07-22       Impact factor: 49.962

10.  Electrically induced bacterial membrane-potential dynamics correspond to cellular proliferation capacity.

Authors:  James P Stratford; Conor L A Edwards; Manjari J Ghanshyam; Dmitry Malyshev; Marco A Delise; Yoshikatsu Hayashi; Munehiro Asally
Journal:  Proc Natl Acad Sci U S A       Date:  2019-04-18       Impact factor: 11.205

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  20 in total

1.  A slime mold's remembrance of things past.

Authors:  Robert H Austin
Journal:  Proc Natl Acad Sci U S A       Date:  2021-04-06       Impact factor: 11.205

2.  Technological Approach to Mind Everywhere: An Experimentally-Grounded Framework for Understanding Diverse Bodies and Minds.

Authors:  Michael Levin
Journal:  Front Syst Neurosci       Date:  2022-03-24

3.  Measurement of the low-frequency charge noise of bacteria.

Authors:  Yichao Yang; Hagen Gress; Kamil L Ekinci
Journal:  Phys Rev E       Date:  2022-06       Impact factor: 2.707

4.  Use of a Fluorescence-Based Assay To Measure Escherichia coli Membrane Potential Changes in High Throughput.

Authors:  M Ashley Hudson; Deborah A Siegele; Steve W Lockless
Journal:  Antimicrob Agents Chemother       Date:  2020-08-20       Impact factor: 5.191

Review 5.  Bistability of somatic pattern memories: stochastic outcomes in bioelectric circuits underlying regeneration.

Authors:  Giovanni Pezzulo; Joshua LaPalme; Fallon Durant; Michael Levin
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-02-08       Impact factor: 6.237

Review 6.  Valuing what happens: a biogenic approach to valence and (potentially) affect.

Authors:  Pamela Lyon; Franz Kuchling
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-01-25       Impact factor: 6.237

7.  Reframing cognition: getting down to biological basics.

Authors:  Pamela Lyon; Fred Keijzer; Detlev Arendt; Michael Levin
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2021-01-25       Impact factor: 6.237

Review 8.  IonoBiology: The functional dynamics of the intracellular metallome, with lessons from bacteria.

Authors:  Leticia Galera-Laporta; Colin J Comerci; Jordi Garcia-Ojalvo; Gürol M Süel
Journal:  Cell Syst       Date:  2021-06-16       Impact factor: 11.091

Review 9.  Unappreciated Roles for K+ Channels in Bacterial Physiology.

Authors:  Sarah D Beagle; Steve W Lockless
Journal:  Trends Microbiol       Date:  2020-12-05       Impact factor: 18.230

Review 10.  Synthetic living machines: A new window on life.

Authors:  Mo R Ebrahimkhani; Michael Levin
Journal:  iScience       Date:  2021-05-04
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