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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 Lab. (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. https://doi.org/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 = {2012},
month = {12}
}

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Works referenced in this record:

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    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