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Inaugural Article

Enzyme leaps fuel antichemotaxis

Ah-Young Jee, Sandipan Dutta, Yoon-Kyoung Cho, View ORCID ProfileTsvi Tlusty, and View ORCID ProfileSteve Granick
PNAS January 2, 2018 115 (1) 14-18; first published December 18, 2017; https://doi.org/10.1073/pnas.1717844115
Ah-Young Jee
aCenter for Soft and Living Matter, Institute for Basic Science, Ulsan 44919, South Korea;
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Sandipan Dutta
aCenter for Soft and Living Matter, Institute for Basic Science, Ulsan 44919, South Korea;
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Yoon-Kyoung Cho
aCenter for Soft and Living Matter, Institute for Basic Science, Ulsan 44919, South Korea;
bDepartment of Biomedical Engineering, Ulsan National Institute of Science and Technology, Ulsan 44919, South Korea;
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Tsvi Tlusty
aCenter for Soft and Living Matter, Institute for Basic Science, Ulsan 44919, South Korea;
cDepartment of Physics, Ulsan National Institute of Science and Technology, Ulsan 44919, South Korea;
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  • ORCID record for Tsvi Tlusty
Steve Granick
aCenter for Soft and Living Matter, Institute for Basic Science, Ulsan 44919, South Korea;
dDepartment of Chemistry, Ulsan National Institute of Science and Technology, Ulsan 44919, South Korea
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  • For correspondence: sgranick@ibs.re.kr
  1. Contributed by Steve Granick, November 10, 2017 (sent for review October 11, 2017; reviewed by Nicholas A. Kotov and Nam Ki Lee)

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Significance

Challenging the traditional view that enzyme kinetics are only a matter of catalyzing chemical reactions, there is mounting evidence that the enzyme catalysis enhances enzyme mobility. This is significant to programming spatio-temporal patterns of molecular response to chemical stimulus, which is common to living matter as well as to significant chemical technology. This paper shows that the enhanced diffusivity of enzymes is a “run-and-tumble” process analogous to that performed by swimming microorganisms, executed in this situation by molecules that lack the decision-making machinery of microorganisms. The result is that enzymes display “antichemotaxis” when they turn over substrate; they migrate in the direction of lesser reactant concentration.

Abstract

There is mounting evidence that enzyme diffusivity is enhanced when the enzyme is catalytically active. Here, using superresolution microscopy [stimulated emission-depletion fluorescence correlation spectroscopy (STED-FCS)], we show that active enzymes migrate spontaneously in the direction of lower substrate concentration (“antichemotaxis”) by a process analogous to the run-and-tumble foraging strategy of swimming microorganisms and our theory quantifies the mechanism. The two enzymes studied, urease and acetylcholinesterase, display two families of transit times through subdiffraction-sized focus spots, a diffusive mode and a ballistic mode, and the latter transit time is close to the inverse rate of catalytic turnover. This biochemical information-processing algorithm may be useful to design synthetic self-propelled swimmers and nanoparticles relevant to active materials. Executed by molecules lacking the decision-making circuitry of microorganisms, antichemotaxis by this run-and-tumble process offers the biological function to homogenize product concentration, which could be significant in situations when the reactant concentration varies from spot to spot.

  • enzyme
  • chemotaxis
  • active matter
  • FCS
  • fluorescence correlation spectroscopy

Footnotes

  • ↵1To whom correspondence should be addressed. Email: sgranick{at}ibs.re.kr.
  • This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2015.

  • Author contributions: A.-Y.J., T.T., and S.G. designed research; A.-Y.J. and S.D. performed research; Y.-K.C. contributed new reagents/analytic tools; A.-Y.J., T.T., and S.G. analyzed data; and A.-Y.J., Y.-K.C., T.T., and S.G. wrote the paper.

  • Reviewers: N.A.K., University of Michigan; and N.K.L., Seoul National University.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1717844115/-/DCSupplemental.

  • Copyright © 2017 the Author(s). Published by PNAS.

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

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Enzyme leaps fuel antichemotaxis
Ah-Young Jee, Sandipan Dutta, Yoon-Kyoung Cho, Tsvi Tlusty, Steve Granick
Proceedings of the National Academy of Sciences Jan 2018, 115 (1) 14-18; DOI: 10.1073/pnas.1717844115

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Enzyme leaps fuel antichemotaxis
Ah-Young Jee, Sandipan Dutta, Yoon-Kyoung Cho, Tsvi Tlusty, Steve Granick
Proceedings of the National Academy of Sciences Jan 2018, 115 (1) 14-18; DOI: 10.1073/pnas.1717844115
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