Logarithmic sensing in Bacillus subtilis aerotaxis

Filippo Menolascina; Roberto Rusconi; Vicente I Fernandez; Steven Smriga; Zahra Aminzare; Eduardo D Sontag; Roman Stocker

doi:10.1038/npjsba.2016.36

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Logarithmic sensing in Bacillus subtilis aerotaxis

Journal article

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Peer reviewed

Logarithmic sensing in Bacillus subtilis aerotaxis

Filippo Menolascina, Roberto Rusconi, Vicente I Fernandez, Steven Smriga, Zahra Aminzare, Eduardo D Sontag and Roman Stocker

NPJ systems biology and applications, Vol.3(1), pp.16036-16036

2017

DOI: 10.1038/npjsba.2016.36

PMCID: PMC5516866

PMID: 28725484

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Abstract

Aerotaxis, the directed migration along oxygen gradients, allows many microorganisms to locate favorable oxygen concentrations. Despite oxygen's fundamental role for life, even key aspects of aerotaxis remain poorly understood. In for example, there is conflicting evidence of whether migration occurs to the maximal oxygen concentration available or to an optimal intermediate one, and how aerotaxis can be maintained over a broad range of conditions. Using precisely controlled oxygen gradients in a microfluidic device, spanning the full spectrum of conditions from quasi-anoxic to oxic (60 n mol/l-1 m mol/l), we resolved 'oxygen preference conundrum' by demonstrating consistent migration towards maximum oxygen concentrations ('monotonic aerotaxis'). Surprisingly, the strength of aerotaxis was largely unchanged over three decades in oxygen concentration (131 n mol/l-196 μ mol/l). We discovered that in this range responds to the logarithm of the oxygen concentration gradient, a rescaling strategy called 'log-sensing' that affords organisms high sensitivity over a wide range of conditions. In these experiments, high-throughput single-cell imaging yielded the best signal-to-noise ratio of any microbial taxis study to date, enabling the robust identification of the first mathematical model for aerotaxis among a broad class of alternative models. The model passed the stringent test of predicting the transient aerotactic response despite being developed on steady-state data, and quantitatively captures both monotonic aerotaxis and log-sensing. Taken together, these results shed new light on the oxygen-seeking capabilities of and provide a blueprint for the quantitative investigation of the many other forms of microbial taxis.

Details

Title: Subtitle: Logarithmic sensing in Bacillus subtilis aerotaxis
Creators: Filippo Menolascina - SynthSys-Centre for Synthetic and Systems Biology, The University of Edinburgh, Scotland, UK
Roberto Rusconi - Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, Zurich, Switzerland
Vicente I Fernandez - Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, Zurich, Switzerland
Steven Smriga - Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, Zurich, Switzerland
Zahra Aminzare - The Program in Applied and Computational Mathematics, Princeton, NJ, USA
Eduardo D Sontag - Department of Mathematics, Hill Center Rutgers, The State University of New Jersey, Piscataway, NJ, USA
Roman Stocker - Institute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, Zurich, Switzerland
Resource Type: Journal article
Publication Details: NPJ systems biology and applications, Vol.3(1), pp.16036-16036
DOI: 10.1038/npjsba.2016.36
PMID: 28725484
PMCID: PMC5516866
NLM abbreviation: NPJ Syst Biol Appl
ISSN: 2056-7189
eISSN: 2056-7189
Publisher: England
Grant note: R01 GM100473 / NIGMS NIH HHS Wellcome Trust
Language: English
Date published: 2017
Academic Unit: Iowa Neuroscience Institute; Mathematics
Record Identifier: 9983985803602771

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