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Title: Interconnected Cavernous Structure of Bacterial Fruiting Bodies

Abstract

The formation of spore-filled fruiting bodies by myxobacteria is a fascinating case of multicelular self-organization by bacteria. The organization of Myxococcus xanthus into fruiting bodies has long been studied not only as an important example of collective motion of bacteria, but also as a simplified model for developmental morphogenesis. Sporulation within the nascent fruiting body requires signaling between moving cells in order that the rod-shaped self-propelled cells differentiate into spores at the appropriate time. Probing the three-dimensional structure of myxobacteria fruiting bodies has previously presented a challenge due to Imitations at different imaging methods. A new technique using Infrared Optical Coherence Tomography (OCT) revealed previously unknown details of the Internal structure of M. xanthus fruiting bodies consisting of interconnected pockets of relative nigh and low spore density regions. Here, to make sense of the experimentally observed structure, modeling and computer simulations were used to test a hypothesized mechanism that could produce high density pockets of spores. The mechanism consists of self-propelled cells aligning with each other and signaling by end-to-end contact to coordinate the process of differentiation resulting in a pattern of clusters observed in the experiment. The Integration of novel OCT experimental techniques with computational simulations can provide newmore » insight Into the mechanisms that can give rise to the pattern formation seen In other biological systems such as dlctyostelids, social amoeba known to form multicellular aggregates observed as slugs under starvation conditions.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [1]
  1. Univ. of Notre Dame, IN (United States). Dept. of Applied and Computational Mathematics and Statistics; Univ. of Notre Dame, IN (United States). Dept. of Physics
  2. Univ. of Notre Dame, IN (United States). Dept. of Applied and Computational Mathematics and Statistics
  3. Stanford Univ., CA (United States). Dept. of Biochemistry
  4. Argonne National Lab. (ANL), Argonne, IL (United States). Materials Science Division; Northwestern Univ., Evanston, IL (United States). Dept. of Engineering Sciences and Applied Mathematics
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
OSTI Identifier:
1396266
Grant/Contract Number:  
AC02-06CH11357; 1R01GM100470-01
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Computational Biology (Online)
Additional Journal Information:
Journal Name: PLoS Computational Biology (Online); Journal Volume: 8; Journal Issue: 12; Journal ID: ISSN 1553-7358
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Harvey, Cameron W., Du, Huijing, Xu, Zhiliang, Kaiser, Dale, Aranson, Igor, and Alber, Mark. Interconnected Cavernous Structure of Bacterial Fruiting Bodies. United States: N. p., 2012. Web. doi:10.1371/journal.pcbi.1002850.
Harvey, Cameron W., Du, Huijing, Xu, Zhiliang, Kaiser, Dale, Aranson, Igor, & Alber, Mark. Interconnected Cavernous Structure of Bacterial Fruiting Bodies. United States. https://doi.org/10.1371/journal.pcbi.1002850
Harvey, Cameron W., Du, Huijing, Xu, Zhiliang, Kaiser, Dale, Aranson, Igor, and Alber, Mark. Thu . "Interconnected Cavernous Structure of Bacterial Fruiting Bodies". United States. https://doi.org/10.1371/journal.pcbi.1002850. https://www.osti.gov/servlets/purl/1396266.
@article{osti_1396266,
title = {Interconnected Cavernous Structure of Bacterial Fruiting Bodies},
author = {Harvey, Cameron W. and Du, Huijing and Xu, Zhiliang and Kaiser, Dale and Aranson, Igor and Alber, Mark},
abstractNote = {The formation of spore-filled fruiting bodies by myxobacteria is a fascinating case of multicelular self-organization by bacteria. The organization of Myxococcus xanthus into fruiting bodies has long been studied not only as an important example of collective motion of bacteria, but also as a simplified model for developmental morphogenesis. Sporulation within the nascent fruiting body requires signaling between moving cells in order that the rod-shaped self-propelled cells differentiate into spores at the appropriate time. Probing the three-dimensional structure of myxobacteria fruiting bodies has previously presented a challenge due to Imitations at different imaging methods. A new technique using Infrared Optical Coherence Tomography (OCT) revealed previously unknown details of the Internal structure of M. xanthus fruiting bodies consisting of interconnected pockets of relative nigh and low spore density regions. Here, to make sense of the experimentally observed structure, modeling and computer simulations were used to test a hypothesized mechanism that could produce high density pockets of spores. The mechanism consists of self-propelled cells aligning with each other and signaling by end-to-end contact to coordinate the process of differentiation resulting in a pattern of clusters observed in the experiment. The Integration of novel OCT experimental techniques with computational simulations can provide new insight Into the mechanisms that can give rise to the pattern formation seen In other biological systems such as dlctyostelids, social amoeba known to form multicellular aggregates observed as slugs under starvation conditions.},
doi = {10.1371/journal.pcbi.1002850},
journal = {PLoS Computational Biology (Online)},
number = 12,
volume = 8,
place = {United States},
year = {Thu Dec 27 00:00:00 EST 2012},
month = {Thu Dec 27 00:00:00 EST 2012}
}

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Works referenced in this record:

Social Interactions in Myxobacterial Swarming
journal, December 2007


Biochemical and structural analyses of the extracellular matrix fibrils of Myxococcus xanthus.
journal, January 1994


Increased Depth of Cellular Imaging in the Intact Lung Using Far-Red and Near-Infrared Fluorescent Probes
journal, January 2006

  • Al-Mehdi, Abu-Bakr; Patel, Mita; Haroon, Abu
  • International Journal of Biomedical Imaging, Vol. 2006
  • DOI: 10.1155/IJBI/2006/37470

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


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


Coupling gene expression and multicellular morphogenesis during fruiting body formation in Myxococcus xanthus: Fruiting body morphogenesis in M. xanthus
journal, March 2003


Developmental waves in myxobacteria: A distinctive pattern formation mechanism
journal, October 2004


A three-dimensional model of myxobacterial fruiting-body formation
journal, November 2006

  • Sozinova, O.; Jiang, Y.; Kaiser, D.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 46
  • DOI: 10.1073/pnas.0605555103

DNA replication during sporulation in Myxococcus xanthus fruiting bodies
journal, September 2005

  • Tzeng, L.; Singer, M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 40
  • DOI: 10.1073/pnas.0506969102

Myxobacteria, Polarity, and Multicellular Morphogenesis
journal, July 2010


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

Gliding motility and polarized slime secretion: Gliding motility and polarized slime secretion
journal, December 2006


Gliding Motility Revisited: How Do the Myxobacteria Move without Flagella?
journal, May 2010

  • Mauriello, E. M. F.; Mignot, T.; Yang, Z.
  • Microbiology and Molecular Biology Reviews, Vol. 74, Issue 2
  • DOI: 10.1128/MMBR.00043-09

Coupling cell movement to multicellular development in myxobacteria
journal, October 2003


Predataxis behavior in Myxococcus xanthus
journal, October 2008

  • Berleman, J. E.; Scott, J.; Chumley, T.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 44
  • DOI: 10.1073/pnas.0804387105

Lipid chemotaxis and signal transduction in Myxococcus xanthus
journal, March 2001


A link between cell movement and gene expression argues that motility is required for cell-cell signaling during fruiting body development.
journal, December 1988


Optical coherence tomography
journal, November 1991


A three-dimensional model of myxobacterial aggregation by contact-mediated interactions
journal, August 2005

  • Sozinova, O.; Jiang, Y.; Kaiser, D.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 32
  • DOI: 10.1073/pnas.0504259102

Extracellular fibrils and contact-mediated cell interactions in Myxococcus xanthus.
journal, January 1991


Cell alignment required in differentiation of Myxococcus xanthus
journal, August 1990


Enhanced mixing and spatial instability in concentrated bacterial suspensions
journal, September 2009

  • Sokolov, Andrey; Goldstein, Raymond E.; Feldchtein, Felix I.
  • Physical Review E, Vol. 80, Issue 3
  • DOI: 10.1103/PhysRevE.80.031903

Refractive Index Determination of Biological Particles
report, July 2006


A three-dimensional model of myxobacterial aggregation by contact-mediated interactions
journal, August 2005

  • Sozinova, O.; Jiang, Y.; Kaiser, D.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 32
  • DOI: 10.1073/pnas.0504259102

DNA replication during sporulation in Myxococcus xanthus fruiting bodies
journal, September 2005

  • Tzeng, L.; Singer, M.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 40
  • DOI: 10.1073/pnas.0506969102

A three-dimensional model of myxobacterial fruiting-body formation
journal, November 2006

  • Sozinova, O.; Jiang, Y.; Kaiser, D.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 46
  • DOI: 10.1073/pnas.0605555103

Predataxis behavior in Myxococcus xanthus
journal, October 2008

  • Berleman, J. E.; Scott, J.; Chumley, T.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 44
  • DOI: 10.1073/pnas.0804387105

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

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


Myxobacteria, Polarity, and Multicellular Morphogenesis
journal, July 2010


A link between cell movement and gene expression argues that motility is required for cell-cell signaling during fruiting body development.
journal, December 1988


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


Optical coherence tomography
journal, November 1991


Genetic Population Structure of the Soil Bacterium Myxococcusxanthus at the Centimeter Scale
journal, May 2006


Myxococcus xanthus Swarms Are Driven by Growth and Regulated by a Pacemaker
journal, August 2011


Are There Lateral as Well as Polar Engines for A-Motile Gliding in Myxobacteria?
journal, July 2009


Autocides produced by Myxococcus xanthus.
journal, January 1984


Extracellular fibrils and contact-mediated cell interactions in Myxococcus xanthus.
journal, January 1991


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


Dynamics of Fruiting Body Morphogenesis
journal, February 2004


Social Interactions in Myxobacterial Swarming
journal, January 2005


Works referencing / citing this record:

An Evo-Devo Perspective on Multicellular Development of Myxobacteria: EVOLUTIONARY PERSPECTIVES ON MYXOBACTERIA DEVELOPMENT
journal, January 2017

  • Arias Del Angel, Juan A.; Escalante, Ana E.; Martínez-Castilla, León Patricio
  • Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, Vol. 328, Issue 1-2
  • DOI: 10.1002/jez.b.22727

Reversals and collisions optimize protein exchange in bacterial swarms
journal, March 2017


Stable emergent formations for a swarm of autonomous car-like vehicles
journal, September 2019