Robustness of a model microbial community emerges from population structure among single cells of a clonal population
Abstract
Microbial populations can withstand, overcome and persist in the face of environmental fluctuation. Previously, we demonstrated how conditional gene regulation in a fluctuating environment drives dilution of condition-specific transcripts, causing a population of Desulfovibrio vulgaris Hildenborough (DvH) to collapse after repeatedly transitioning from sulfate respiration to syntrophic conditions with the methanogen Methanococcus maripaludis. Failure of the DvH to successfully transition contributed to the collapse of this model community. We investigated the mechanistic basis for loss of robustness by examining whether conditional gene regulation altered heterogeneity in gene expression across individual DvH cells. We discovered that robustness of a microbial population across environmental transitions was attributable to the retention of cells in two states that exhibited different condition-specific gene expression patterns. In our experiments, a population with disrupted conditional regulation successfully alternated between cell states. Meanwhile, a population with intact conditional regulation successfully switched between cell states initially, but collapsed after repeated transitions, possibly due to the high energy requirements of regulation. These results demonstrate that the survival of this entire model microbial community is dependent on the regulatory system's influence on the distribution of distinct cell states among individual cells within a clonal population.
- Authors:
-
- Institute for Systems Biology, Seattle, WA (United States)
- Univ. of Washington, Seattle, WA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1777942
- Alternate Identifier(s):
- OSTI ID: 1375466
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 19; Journal Issue: 8; Journal ID: ISSN 1462-2912
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; single cell; robustness; gene expression; Desulfovibrio; syntrophy; sulfate respiration
Citation Formats
Thompson, Anne W., Turkarslan, Serdar, Arens, Christina E., López García de Lomana, Adrián, Raman, Arjun V., Stahl, David A., and Baliga, Nitin S. Robustness of a model microbial community emerges from population structure among single cells of a clonal population. United States: N. p., 2017.
Web. doi:10.1111/1462-2920.13764.
Thompson, Anne W., Turkarslan, Serdar, Arens, Christina E., López García de Lomana, Adrián, Raman, Arjun V., Stahl, David A., & Baliga, Nitin S. Robustness of a model microbial community emerges from population structure among single cells of a clonal population. United States. https://doi.org/10.1111/1462-2920.13764
Thompson, Anne W., Turkarslan, Serdar, Arens, Christina E., López García de Lomana, Adrián, Raman, Arjun V., Stahl, David A., and Baliga, Nitin S. Mon .
"Robustness of a model microbial community emerges from population structure among single cells of a clonal population". United States. https://doi.org/10.1111/1462-2920.13764. https://www.osti.gov/servlets/purl/1777942.
@article{osti_1777942,
title = {Robustness of a model microbial community emerges from population structure among single cells of a clonal population},
author = {Thompson, Anne W. and Turkarslan, Serdar and Arens, Christina E. and López García de Lomana, Adrián and Raman, Arjun V. and Stahl, David A. and Baliga, Nitin S.},
abstractNote = {Microbial populations can withstand, overcome and persist in the face of environmental fluctuation. Previously, we demonstrated how conditional gene regulation in a fluctuating environment drives dilution of condition-specific transcripts, causing a population of Desulfovibrio vulgaris Hildenborough (DvH) to collapse after repeatedly transitioning from sulfate respiration to syntrophic conditions with the methanogen Methanococcus maripaludis. Failure of the DvH to successfully transition contributed to the collapse of this model community. We investigated the mechanistic basis for loss of robustness by examining whether conditional gene regulation altered heterogeneity in gene expression across individual DvH cells. We discovered that robustness of a microbial population across environmental transitions was attributable to the retention of cells in two states that exhibited different condition-specific gene expression patterns. In our experiments, a population with disrupted conditional regulation successfully alternated between cell states. Meanwhile, a population with intact conditional regulation successfully switched between cell states initially, but collapsed after repeated transitions, possibly due to the high energy requirements of regulation. These results demonstrate that the survival of this entire model microbial community is dependent on the regulatory system's influence on the distribution of distinct cell states among individual cells within a clonal population.},
doi = {10.1111/1462-2920.13764},
journal = {Environmental Microbiology},
number = 8,
volume = 19,
place = {United States},
year = {Mon Apr 17 00:00:00 EDT 2017},
month = {Mon Apr 17 00:00:00 EDT 2017}
}
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