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Title: Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior

Abstract

The myxobacteria are a family of soil bacteria that form biofilms of complex architecture, aligned multilayered swarms or fruiting body structures that are simple or branched aggregates containing myxospores. Here, we examined the structural role of matrix exopolysaccharide (EPS) in the organization of these surface-dwelling bacterial cells. Using time-lapse light and fluorescence microscopy, as well as transmission electron microscopy and focused ion beam/scanning electron microscopy (FIB/SEM) electron microscopy, we found that Myxococcus xanthus cell organization in biofilms is dependent on the formation of EPS microchannels. Cells are highly organized within the three-dimensional structure of EPS microchannels that are required for cell alignment and advancement on surfaces. Mutants lacking EPS showed a lack of cell orientation and poor colony migration. Purified, cell-free EPS retains a channel-like structure, and can complement EPS - mutant motility defects. In addition, EPS provides the cooperative structure for fruiting body formation in both the simple mounds of M. xanthus and the complex, tree-like structures of Chondromyces crocatus. We furthermore investigated the possibility that EPS impacts community structure as a shared resource facilitating cooperative migration among closely related isolates of M. xanthus.

Authors:
 [1];  [2];  [2];  [3];  [4];  [5];  [5];  [2];  [4];  [2];  [6];  [2];  [4];  [2]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); St. Mary's College, Moraga, CA (United States); Univ. of California, Berkeley, CA (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Univ. of California, Berkeley, CA (United States); Shandong Univ., Jinan (China)
  4. Univ. of California, Berkeley, CA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); St. Mary's College, Moraga, CA (United States)
  6. FEI, Inc., Hillsboro, OR (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1377561
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 10; Journal Issue: 11; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Berleman, James E., Zemla, Marcin, Remis, Jonathan P., Liu, Hong, Davis, Annie E., Worth, Alexandra N., West, Zachary, Zhang, Angela, Park, Hanwool, Bosneaga, Elena, van Leer, Brandon, Tsai, Wenting, Zusman, David R., and Auer, Manfred. Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior. United States: N. p., 2016. Web. doi:10.1038/ismej.2016.60.
Berleman, James E., Zemla, Marcin, Remis, Jonathan P., Liu, Hong, Davis, Annie E., Worth, Alexandra N., West, Zachary, Zhang, Angela, Park, Hanwool, Bosneaga, Elena, van Leer, Brandon, Tsai, Wenting, Zusman, David R., & Auer, Manfred. Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior. United States. doi:10.1038/ismej.2016.60.
Berleman, James E., Zemla, Marcin, Remis, Jonathan P., Liu, Hong, Davis, Annie E., Worth, Alexandra N., West, Zachary, Zhang, Angela, Park, Hanwool, Bosneaga, Elena, van Leer, Brandon, Tsai, Wenting, Zusman, David R., and Auer, Manfred. Fri . "Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior". United States. doi:10.1038/ismej.2016.60. https://www.osti.gov/servlets/purl/1377561.
@article{osti_1377561,
title = {Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior},
author = {Berleman, James E. and Zemla, Marcin and Remis, Jonathan P. and Liu, Hong and Davis, Annie E. and Worth, Alexandra N. and West, Zachary and Zhang, Angela and Park, Hanwool and Bosneaga, Elena and van Leer, Brandon and Tsai, Wenting and Zusman, David R. and Auer, Manfred},
abstractNote = {The myxobacteria are a family of soil bacteria that form biofilms of complex architecture, aligned multilayered swarms or fruiting body structures that are simple or branched aggregates containing myxospores. Here, we examined the structural role of matrix exopolysaccharide (EPS) in the organization of these surface-dwelling bacterial cells. Using time-lapse light and fluorescence microscopy, as well as transmission electron microscopy and focused ion beam/scanning electron microscopy (FIB/SEM) electron microscopy, we found that Myxococcus xanthus cell organization in biofilms is dependent on the formation of EPS microchannels. Cells are highly organized within the three-dimensional structure of EPS microchannels that are required for cell alignment and advancement on surfaces. Mutants lacking EPS showed a lack of cell orientation and poor colony migration. Purified, cell-free EPS retains a channel-like structure, and can complement EPS - mutant motility defects. In addition, EPS provides the cooperative structure for fruiting body formation in both the simple mounds of M. xanthus and the complex, tree-like structures of Chondromyces crocatus. We furthermore investigated the possibility that EPS impacts community structure as a shared resource facilitating cooperative migration among closely related isolates of M. xanthus.},
doi = {10.1038/ismej.2016.60},
journal = {The ISME Journal},
number = 11,
volume = 10,
place = {United States},
year = {2016},
month = {5}
}

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