Bacteria Floc, but Do They Flock? Insights from Population Interaction Models of Quorum Sensing

Hana Ueda; Kristina Stephens; Konstantina Trivisa; William E Bentley

doi:10.1128/mBio.00972-19

Bacteria Floc, but Do They Flock? Insights from Population Interaction Models of Quorum Sensing

mBio. 2019 May 28;10(3):e00972-19. doi: 10.1128/mBio.00972-19.

Authors

Hana Ueda^{1

2

3

4}, Kristina Stephens^{3

4}, Konstantina Trivisa^{1

2}, William E Bentley^{5

3

4}

Affiliations

¹ Department of Mathematics, University of Maryland College Park, College Park, Maryland, USA.
² Graduate Program in Applied Mathematics & Statistics, and Scientific Computation, University of Maryland College Park, College Park, Maryland, USA.
³ Fischell Department of Bioengineering, University of Maryland College Park, College Park, Maryland, USA.
⁴ Institute for Bioscience and Biotechnology Research, University of Maryland, College Park, Maryland, USA.
⁵ Graduate Program in Applied Mathematics & Statistics, and Scientific Computation, University of Maryland College Park, College Park, Maryland, USA bentley@umd.edu.

Abstract

Quorum sensing (QS) enables coordinated, population-wide behavior. QS-active bacteria "communicate" their number density using autoinducers which they synthesize, collect, and interpret. Tangentially, chemotactic bacteria migrate, seeking out nutrients and other molecules. It has long been hypothesized that bacterial behaviors, such as chemotaxis, were the primordial progenitors of complex behaviors of higher-order organisms. Recently, QS was linked to chemotaxis, yet the notion that these behaviors can together contribute to higher-order behaviors has not been shown. Here, we mathematically link flocking behavior, commonly observed in fish and birds, to bacterial chemotaxis and QS by constructing a phenomenological model of population-scale QS-mediated phenomena. Specifically, we recast a previously developed mathematical model of flocking and found that simulated bacterial behaviors aligned well with well-known QS behaviors. This relatively simple system of ordinary differential equations affords analytical analysis of asymptotic behavior and describes cell position and velocity, QS-mediated protein expression, and the surrounding concentrations of an autoinducer. Further, heuristic explorations of the model revealed that the emergence of "migratory" subpopulations occurs only when chemotaxis is directly linked to QS. That is, behaviors were simulated when chemotaxis was coupled to QS and when not. When coupled, the bacterial flocking model predicts the formation of two distinct groups of cells migrating at different speeds in their journey toward an attractant. This is qualitatively similar to phenomena spotted in our Escherichiacoli chemotaxis experiments as well as in analogous work observed over 50 years ago.IMPORTANCE Our modeling efforts show how cell density can affect chemotaxis; they help to explain the roots of subgroup formation in bacterial populations. Our work also reinforces the notion that bacterial mechanisms are at times exhibited in higher-order organisms.

Keywords: chemotaxis; flocking; quorum sensing.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Bacterial Physiological Phenomena*
Chemotaxis*
Escherichia coli / physiology
Models, Biological
Models, Theoretical*
Quorum Sensing*

Abstract

Publication types

MeSH terms

Grants and funding