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Self-Organization, Layered Structure, and Aggregation Enhance Persistence of a Synthetic Biofilm Consortium

Brenner, Katie and Arnold, Frances H. (2011) Self-Organization, Layered Structure, and Aggregation Enhance Persistence of a Synthetic Biofilm Consortium. PLoS ONE, 6 (2). Art. No. e16791 . ISSN 1932-6203. PMCID PMC3036657. doi:10.1371/journal.pone.0016791. https://resolver.caltech.edu/CaltechAUTHORS:20110307-110900429

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Abstract

Microbial consortia constitute a majority of the earth’s biomass, but little is known about how these cooperating communities persist despite competition among community members. Theory suggests that non-random spatial structures contribute to the persistence of mixed communities; when particular structures form, they may provide associated community members with a growth advantage over unassociated members. If true, this has implications for the rise and persistence of multi-cellular organisms. However, this theory is difficult to study because we rarely observe initial instances of non-random physical structure in natural populations. Using two engineered strains of Escherichia coli that constitute a synthetic symbiotic microbial consortium, we fortuitously observed such spatial self-organization. This consortium forms a biofilm and, after several days, adopts a defined layered structure that is associated with two unexpected, measurable growth advantages. First, the consortium cannot successfully colonize a new, downstream environment until it selforganizes in the initial environment; in other words, the structure enhances the ability of the consortium to survive environmental disruptions. Second, when the layered structure forms in downstream environments the consortium accumulates significantly more biomass than it did in the initial environment; in other words, the structure enhances the global productivity of the consortium. We also observed that the layered structure only assembles in downstream environments that are colonized by aggregates from a previous, structured community. These results demonstrate roles for self-organization and aggregation in persistence of multi-cellular communities, and also illustrate a role for the techniques of synthetic biology in elucidating fundamental biological principles.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1371/journal.pone.0016791 DOIArticle
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0016791PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3036657/PubMed CentralArticle
ORCID:
AuthorORCID
Arnold, Frances H.0000-0002-4027-364X
Additional Information:© 2011 Brenner, Arnold. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received August 27, 2010; Accepted January 12, 2011; Published February 9, 2011. Editor: Najib El-Sayed, The University of Maryland, United States of America. Funding: The work was supported by the National Institutes of Health grant 1-R01-CA118486. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors thank Lingchong You and Ron Weiss for comments on the manuscript, and the Caltech Biological Imaging and Flow Cytometry Centers. Author Contributions: Conceived and designed the experiments: KB. Performed the experiments: KB. Analyzed the data: KB FHA. Contributed reagents/materials/analysis tools: KB FHA. Wrote the paper: KB FHA.
Funders:
Funding AgencyGrant Number
NIH1-R01-CA118486
Issue or Number:2
PubMed Central ID:PMC3036657
DOI:10.1371/journal.pone.0016791
Record Number:CaltechAUTHORS:20110307-110900429
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20110307-110900429
Official Citation:Brenner K, Arnold FH (2011) Self-Organization, Layered Structure, and Aggregation Enhance Persistence of a Synthetic Biofilm Consortium. PLoS ONE 6(2): e16791. doi:10.1371/journal.pone.0016791
Usage Policy:This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
ID Code:22688
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:08 Mar 2011 18:31
Last Modified:09 Nov 2021 16:07

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