Coupling between distant biofilms and emergence of nutrient time-sharing

Jintao Liu, Rosa Martinez-Corral, Arthur Prindle, Dong Yeon D. Lee, Joseph Larkin, Marçal Gabalda-Sagarra, Jordi Garcia-Ojalvo, Gürol M. Süel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

181 Scopus citations

Abstract

Bacteria within communities can interact to organize their behavior. It has been unclear whether such interactions can extend beyond a single community to coordinate the behavior of distant populations. We discovered that two Bacillus subtilis biofilm communities undergoing metabolic oscillations can become coupled through electrical signaling and synchronize their growth dynamics. Coupling increases competition by also synchronizing demand for limited nutrients. As predicted by mathematical modeling, we confirm that biofilms resolve this conflict by switching from in-phase to antiphase oscillations. This results in time-sharing behavior, where each community takes turns consuming nutrients. Time-sharing enables biofilms to counterintuitively increase growth under reduced nutrient supply. Distant biofilms can thus coordinate their behavior to resolve nutrient competition through time-sharing, a strategy used in engineered systems to allocate limited resources.

Original languageEnglish (US)
Pages (from-to)638-642
Number of pages5
JournalScience
Volume356
Issue number6338
DOIs
StatePublished - May 12 2017

Funding

We thank M. Asally, T. Çaǧatay, M. Elowitz, T. Hwa, S. Lockless, K. Süel, M. Vergassola, and R. Wollman for comments during the writing of the manuscript. This work was in part supported by the San Diego Center for Systems Biology (NIH grant P50 GM085764), the National Institute of General Medical Sciences (grant R01 GM121888 to G.M.S.), the Defense Advanced Research Projects Agency (grant HR0011-16-2-0035 to G.M.S.), the Howard Hughes Medical Institute-Simons Foundation Faculty Scholars program (to G.M.S.), a Simons Foundation Fellowship of the Helen Hay Whitney Foundation (to A.P.), a Career Award at the Scientific Interface from the Burroughs Wellcome Fund (to A.P.), the Spanish Ministry of Economy and Competitiveness and FEDER (European Regional Development Fund) (project FIS2015-66503-C3-1-P, to J.G.-O.), the Generalitat de Catalunya (project 2014SGR0947, to J.G.-O.), the ICREA (Catalan Institution for Research and Advanced Studies) Academia program (to J.G.-O.), the "Maria de Maeztu" Programme for Units of Excellence in Research and Development (Spanish Ministry of Economy and Competitiveness, grant MDM-2014-0370 to J.G.-O.), the La Caixa foundation (to R.M.-C.), and a doctoral grant from the Formacion del Profesorado Universitario program of the Ministerio de Educacion, Cultura y Deportes, Spain (to M.G.-S.).

ASJC Scopus subject areas

  • General

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