Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior

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

doi:10.1038/ismej.2016.60

Title: Exopolysaccharide microchannels direct bacterial motility and organize multicellular behavior

Journal Article · Fri May 06 00:00:00 EDT 2016 · The ISME Journal

DOI: https://doi.org/10.1038/ismej.2016.60 · OSTI ID:1377561

Berleman, James E. ^[1]; Zemla, Marcin ^[2]; Remis, Jonathan P. ^[2]; Liu, Hong ^[3]; Davis, Annie E. ^[4]; Worth, Alexandra N. ^[5]; West, Zachary ^[5]; Zhang, Angela ^[2]; Park, Hanwool ^[4]; Bosneaga, Elena ^[2]; van Leer, Brandon ^[6]; Tsai, Wenting ^[2]; Zusman, David R. ^[4]; Auer, Manfred ^[2]

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); St. Mary's College, Moraga, CA (United States); Univ. of California, Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Shandong Univ., Jinan (China)
Univ. of California, Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); St. Mary's College, Moraga, CA (United States)
FEI, Inc., Hillsboro, OR (United States)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1377561

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 11 Vol. 10; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Agent-Based Modeling Reveals Possible Mechanisms for Observed Aggregation Cell Behaviors in Myxococcus xanthus Zhang, Zhaoyang; Igoshin, Oleg A.; Cotter, Christopher R. bioRxiv https://doi.org/10.1101/320291	posted_content	May 2018
Spatial Organization Plasticity as an Adaptive Driver of Surface Microbial Communities Bridier, Arnaud; Piard, Jean-Christophe; Pandin, Caroline Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01364	journal	July 2017
Geometrical Distribution of Cryptococcus neoformans Mediates Flower-Like Biofilm Development Lopes, William; Vainstein, Mendeli H.; De Sousa Araujo, Glauber R. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02534	journal	December 2017
Cryptococcal Traits Mediating Adherence to Biotic and Abiotic Surfaces Camacho, Emma; Casadevall, Arturo Journal of Fungi, Vol. 4, Issue 3 https://doi.org/10.3390/jof4030088	journal	July 2018
Two genomic regions encoding exopolysaccharide production systems have complementary functions in B. cereus multicellularity and host interaction Caro-Astorga, Joaquin; Álvarez-Mena, Ana; Hierrezuelo, Jesús Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57970-3	journal	January 2020
Exopolysaccharide protects Vibrio cholerae from exogenous attacks by the type 6 secretion system Toska, Jonida; Ho, Brian T.; Mekalanos, John J. Proceedings of the National Academy of Sciences, Vol. 115, Issue 31 https://doi.org/10.1073/pnas.1808469115	journal	July 2018
Biophysical processes supporting the diversity of microbial life in soil Tecon, Robin; Or, Dani FEMS Microbiology Reviews, Vol. 41, Issue 5 https://doi.org/10.1093/femsre/fux039	journal	August 2017
Agent-Based Modeling Reveals Possible Mechanisms for Observed Aggregation Cell Behaviors in Myxococcus xanthus Zhang, Zhaoyang; Igoshin, Oleg A.; Cotter, Christopher R. bioRxiv https://doi.org/10.1101/320291	posted_content	May 2018
Exopolysaccharides promote Myxococcus xanthus social motility by inhibiting cellular reversals: EPS regulates cellular reversals in myxobacteria Zhou, Tianyi; Nan, Beiyan Molecular Microbiology, Vol. 103, Issue 4 https://doi.org/10.1111/mmi.13585	journal	December 2016
Galactose Metabolism Plays a Crucial Role in Biofilm Formation by Bacillus subtilis Chai, Yunrong; Beauregard, Pascale B.; Vlamakis, Hera mBio, Vol. 3, Issue 4 https://doi.org/10.1128/mBio.00184-12	journal	August 2012
Spatial Organization Plasticity as an Adaptive Driver of Surface Microbial Communities Bridier, Arnaud; Piard, Jean-Christophe; Pandin, Caroline Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01364	journal	July 2017
Geometrical Distribution of Cryptococcus neoformans Mediates Flower-Like Biofilm Development Lopes, William; Vainstein, Mendeli H.; De Sousa Araujo, Glauber R. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02534	journal	December 2017
Cryptococcal Traits Mediating Adherence to Biotic and Abiotic Surfaces Camacho, Emma; Casadevall, Arturo Journal of Fungi, Vol. 4, Issue 3 https://doi.org/10.3390/jof4030088	journal	July 2018
Biophysical processes supporting the diversity of microbial life in soil Robin, Tecon,; Dani, Or, ETH Zurich https://doi.org/10.3929/ethz-b-000219910	text	January 2017

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