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Title: Reversals and collisions optimize protein exchange in bacterial swarms

Abstract

Swarming groups of bacteria coordinate their behavior by self-organizing as a population to move over surfaces in search of nutrients and optimal niches for colonization. Many open questions remain about the cues used by swarming bacteria to achieve this self-organization. While chemical cue signaling known as quorum sensing is well-described, swarming bacteria often act and coordinate on time scales that could not be achieved via these extracellular quorum sensing cues. Here, cell-cell contact-dependent protein exchange is explored as amechanism of intercellular signaling for the bacterium Myxococcus xanthus. A detailed biologically calibrated computational model is used to study how M. xanthus optimizes the connection rate between cells and maximizes the spread of an extracellular protein within the population. The maximum rate of protein spreading is observed for cells that reverse direction optimally for swarming. Cells that reverse too slowly or too fast fail to spread extracellular protein efficiently. In particular, a specific range of cell reversal frequencies was observed to maximize the cell-cell connection rate and minimize the time of protein spreading. Furthermore, our findings suggest that predesigned motion reversal can be employed to enhance the collective behavior of biological synthetic active systems.

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science - Office of Basic Energy Sciences - Materials Sciences and Engineering Division; National Institutes of Health (NIH)
OSTI Identifier:
1366715
DOE Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article
Journal Name:
Physical Review E
Additional Journal Information:
Journal Volume: 95; Journal Issue: 3; Journal ID: ISSN 2470-0045
Publisher:
American Physical Society (APS)
Country of Publication:
United States
Language:
English

Citation Formats

Amiri, Aboutaleb, Harvey, Cameron, Buchmann, Amy, Christley, Scott, Shrout, Joshua D., Aranson, Igor S., and Alber, Mark. Reversals and collisions optimize protein exchange in bacterial swarms. United States: N. p., 2017. Web. doi:10.1103/PhysRevE.95.032408.
Amiri, Aboutaleb, Harvey, Cameron, Buchmann, Amy, Christley, Scott, Shrout, Joshua D., Aranson, Igor S., & Alber, Mark. Reversals and collisions optimize protein exchange in bacterial swarms. United States. doi:10.1103/PhysRevE.95.032408.
Amiri, Aboutaleb, Harvey, Cameron, Buchmann, Amy, Christley, Scott, Shrout, Joshua D., Aranson, Igor S., and Alber, Mark. Wed . "Reversals and collisions optimize protein exchange in bacterial swarms". United States. doi:10.1103/PhysRevE.95.032408.
@article{osti_1366715,
title = {Reversals and collisions optimize protein exchange in bacterial swarms},
author = {Amiri, Aboutaleb and Harvey, Cameron and Buchmann, Amy and Christley, Scott and Shrout, Joshua D. and Aranson, Igor S. and Alber, Mark},
abstractNote = {Swarming groups of bacteria coordinate their behavior by self-organizing as a population to move over surfaces in search of nutrients and optimal niches for colonization. Many open questions remain about the cues used by swarming bacteria to achieve this self-organization. While chemical cue signaling known as quorum sensing is well-described, swarming bacteria often act and coordinate on time scales that could not be achieved via these extracellular quorum sensing cues. Here, cell-cell contact-dependent protein exchange is explored as amechanism of intercellular signaling for the bacterium Myxococcus xanthus. A detailed biologically calibrated computational model is used to study how M. xanthus optimizes the connection rate between cells and maximizes the spread of an extracellular protein within the population. The maximum rate of protein spreading is observed for cells that reverse direction optimally for swarming. Cells that reverse too slowly or too fast fail to spread extracellular protein efficiently. In particular, a specific range of cell reversal frequencies was observed to maximize the cell-cell connection rate and minimize the time of protein spreading. Furthermore, our findings suggest that predesigned motion reversal can be employed to enhance the collective behavior of biological synthetic active systems.},
doi = {10.1103/PhysRevE.95.032408},
journal = {Physical Review E},
issn = {2470-0045},
number = 3,
volume = 95,
place = {United States},
year = {2017},
month = {3}
}

Works referenced in this record:

A Mathematical Theory of Communication
journal, July 1948


The tgl gene: social motility and stimulation in Myxococcus xanthus.
journal, July 1997


Mechanism for Collective Cell Alignment in Myxococcus xanthus Bacteria
journal, August 2015


Interconnected Cavernous Structure of Bacterial Fruiting Bodies
journal, December 2012


The application of information theory to biochemical signaling systems
journal, August 2012


Collective motion
journal, August 2012


Theoretical approaches to the steady-state statistical physics of interacting dissipative units
journal, January 2017


Three-dimensional multi-scale model of deformable platelets adhesion to vessel wall in blood flow
journal, August 2014

  • Wu, Ziheng; Xu, Zhiliang; Kim, Oleg
  • Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 372, Issue 2021
  • DOI: 10.1098/rsta.2013.0380

Biodirected epitaxial nanodeposition of polymers on oriented macromolecular templates
journal, October 2002

  • Kondo, T.; Nojiri, M.; Hishikawa, Y.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 22
  • DOI: 10.1073/pnas.212238399

Modelling platelet–blood flow interaction using the subcellular element Langevin method
journal, May 2011

  • Sweet, Christopher R.; Chatterjee, Santanu; Xu, Zhiliang
  • Journal of The Royal Society Interface, Vol. 8, Issue 65
  • DOI: 10.1098/rsif.2011.0180

Collective Motion and Nonequilibrium Cluster Formation in Colonies of Gliding Bacteria
journal, February 2012


Heterologous protein transfer within structured myxobacteria biofilms: Lipoprotein transfer in myxobacteria
journal, June 2011


Intercellular C-signaling and the traveling waves of Myxococcus.
journal, December 1994


The lethal cargo of Myxococcus xanthus outer membrane vesicles
journal, September 2014

  • Berleman, James E.; Allen, Simon; Danielewicz, Megan A.
  • Frontiers in Microbiology, Vol. 5
  • DOI: 10.3389/fmicb.2014.00474

Cluster dynamics and cluster size distributions in systems of self-propelled particles
journal, December 2010

  • Peruani, F.; Schimansky-Geier, L.; Bär, M.
  • The European Physical Journal Special Topics, Vol. 191, Issue 1
  • DOI: 10.1140/epjst/e2010-01349-1

Study of elastic collisions of Myxococcus xanthus in swarms
journal, April 2011


Cell rejuvenation and social behaviors promoted by LPS exchange in myxobacteria
journal, May 2015

  • Vassallo, Christopher; Pathak, Darshankumar T.; Cao, Pengbo
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 22
  • DOI: 10.1073/pnas.1503553112

Meso-scale turbulence in living fluids
journal, August 2012

  • Wensink, H. H.; Dunkel, J.; Heidenreich, S.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 36
  • DOI: 10.1073/pnas.1202032109

Cell Contact–Dependent Outer Membrane Exchange in Myxobacteria: Genetic Determinants and Mechanism
journal, April 2012


Towards a unifying approach to diversity measures: Bridging the gap between the Shannon entropy and Rao's quadratic index
journal, November 2006


Direct live imaging of cell–cell protein transfer by transient outer membrane fusion in Myxococcus xanthus
journal, July 2013


Periodic Reversals in Paenibacillus dendritiformis Swarming
journal, April 2013

  • Be'er, A.; Strain, S. K.; Hernandez, R. A.
  • Journal of Bacteriology, Vol. 195, Issue 12
  • DOI: 10.1128/JB.00080-13

Periodic reversal of direction allows Myxobacteria to swarm
journal, January 2009

  • Wu, Y.; Kaiser, A. D.; Jiang, Y.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 4
  • DOI: 10.1073/pnas.0811662106

The Mechanistic Basis of Myxococcus xanthus Rippling Behavior and Its Physiological Role during Predation
journal, September 2012


Type IV pili interactions promote intercellular association and moderate swarming of Pseudomonas aeruginosa
journal, December 2014

  • Anyan, Morgen E.; Amiri, Aboutaleb; Harvey, Cameron W.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 50
  • DOI: 10.1073/pnas.1414661111

Self-organization of bacterial biofilms is facilitated by extracellular DNA
journal, June 2013

  • Gloag, E. S.; Turnbull, L.; Huang, A.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 28
  • DOI: 10.1073/pnas.1218898110

Integrative multicellular biological modeling: a case study of 3D epidermal development using GPU algorithms
journal, August 2010


Predatory activity of Myxococcus xanthus outer-membrane vesicles and properties of their hydrolase cargo
journal, September 2012


Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy
journal, April 2005

  • Pelling, A. E.; Li, Y.; Shi, W.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 18
  • DOI: 10.1073/pnas.0501207102

Bayesian Inference for Identifying Interaction Rules in Moving Animal Groups
journal, August 2011


Aerotaxis in Halobacterium salinarium is methylation-dependent
journal, November 1995


How Myxobacteria Cooperate
journal, November 2015

  • Cao, Pengbo; Dey, Arup; Vassallo, Christopher N.
  • Journal of Molecular Biology, Vol. 427, Issue 23
  • DOI: 10.1016/j.jmb.2015.07.022

Heterogeneous Diversity of Spacers within CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats)
journal, September 2010


Dynamics of Bacterial Swarming
journal, May 2010

  • Darnton, Nicholas C.; Turner, Linda; Rojevsky, Svetlana
  • Biophysical Journal, Vol. 98, Issue 10
  • DOI: 10.1016/j.bpj.2010.01.053

Modeling Multicellular Systems Using Subcellular Elements
journal, August 2005


A Common Step for Changing Cell Shape in Fruiting Body and Starvation-Independent Sporulation of Myxococcus xanthus
journal, June 2000


Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus
journal, July 1977

  • Hodgkin, J.; Kaiser, D.
  • Proceedings of the National Academy of Sciences, Vol. 74, Issue 7
  • DOI: 10.1073/pnas.74.7.2938

Bird Flocks as Condensed Matter
journal, March 2014


Genetics of gliding motility in Myxococcus xanthus (Myxobacterales): Genes controlling movement of single cells
journal, January 1979

  • Hodgkin, Jonathan; Kaiser, Dale
  • MGG Molecular & General Genetics, Vol. 171, Issue 2
  • DOI: 10.1007/BF00270003

"Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility.
journal, December 1985

  • Blackhart, B. D.; Zusman, D. R.
  • Proceedings of the National Academy of Sciences, Vol. 82, Issue 24
  • DOI: 10.1073/pnas.82.24.8767

Cell-to-Cell Transfer of Bacterial Outer Membrane Lipoproteins
journal, July 2005


Contact- and Protein Transfer-Dependent Stimulation of Assembly of the Gliding Motility Machinery in Myxococcus xanthus
journal, July 2015


Collective Swimming and the Dynamics of Bacterial Turbulence
journal, August 2008


Myxococcus xanthus Gliding Motors Are Elastically Coupled to the Substrate as Predicted by the Focal Adhesion Model of Gliding Motility
journal, May 2014


Self-propelled rods exhibit a phase-separated state characterized by the presence of active stresses and the ejection of polar clusters
journal, July 2015