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Mol Syst Biol. 2017 Mar 20;13(3):919. doi: 10.15252/msb.20167058.

Mechanism for microbial population collapse in a fluctuating resource environment.

Author information

1
Institute for Systems Biology, Seattle, WA, USA.
2
Civil and Environmental Engineering, University of Washington, Seattle, WA, USA.
3
Biological Sciences, University of Washington Bothell, Bothell, WA, USA.
4
Earth and Space Sciences, University of Washington, Seattle, WA, USA.
5
Department of Biochemistry, University of Missouri, Columbia, MO, USA.
6
Institute for Systems Biology, Seattle, WA, USA nbaliga@systemsbiology.org.

Abstract

Managing trade-offs through gene regulation is believed to confer resilience to a microbial community in a fluctuating resource environment. To investigate this hypothesis, we imposed a fluctuating environment that required the sulfate-reducer Desulfovibrio vulgaris to undergo repeated ecologically relevant shifts between retaining metabolic independence (active capacity for sulfate respiration) and becoming metabolically specialized to a mutualistic association with the hydrogen-consuming Methanococcus maripaludis Strikingly, the microbial community became progressively less proficient at restoring the environmentally relevant physiological state after each perturbation and most cultures collapsed within 3-7 shifts. Counterintuitively, the collapse phenomenon was prevented by a single regulatory mutation. We have characterized the mechanism for collapse by conducting RNA-seq analysis, proteomics, microcalorimetry, and single-cell transcriptome analysis. We demonstrate that the collapse was caused by conditional gene regulation, which drove precipitous decline in intracellular abundance of essential transcripts and proteins, imposing greater energetic burden of regulation to restore function in a fluctuating environment.

KEYWORDS:

fluctuating resource environment; microbial population collapse; regulation; resilience; syntrophy

PMID:
28320772
PMCID:
PMC5371734
DOI:
10.15252/msb.20167058
[Indexed for MEDLINE]
Free PMC Article

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