Mechanism for microbial population collapse in a fluctuating resource environment.
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-reducerDesulfovibrio vulgaristo 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-consumingMethanococcus maripaludisStrikingly, 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.
Institute for Systems Biology, Seattle, WA, USA.
Serdar
0000-0003-1679-6405
S
Turkarslan
Institute for Systems Biology, Seattle, WA, USA.
Arjun V
AV
Raman
Institute for Systems Biology, Seattle, WA, USA.
Anne W
AW
Thompson
Institute for Systems Biology, Seattle, WA, USA.
Christina E
CE
Arens
Institute for Systems Biology, Seattle, WA, USA.
Mark A
MA
Gillespie
Civil and Environmental Engineering, University of Washington, Seattle, WA, USA.
Frederick
F
von Netzer
Biological Sciences, University of Washington Bothell, Bothell, WA, USA.
Kristina L
KL
Hillesland
Institute for Systems Biology, Seattle, WA, USA.
Sergey
S
Stolyar
Institute for Systems Biology, Seattle, WA, USA.
Adrian
A
López García de Lomana
Institute for Systems Biology, Seattle, WA, USA.
David J
DJ
Reiss
Earth and Space Sciences, University of Washington, Seattle, WA, USA.
Drew
D
Gorman-Lewis
Department of Biochemistry, University of Missouri, Columbia, MO, USA.
Grant M
GM
Zane
Institute for Systems Biology, Seattle, WA, USA.
Jeffrey A
JA
Ranish
Department of Biochemistry, University of Missouri, Columbia, MO, USA.
Judy D
JD
Wall
Civil and Environmental Engineering, University of Washington, Seattle, WA, USA.
David A
DA
Stahl
Institute for Systems Biology, Seattle, WA, USA nbaliga@systemsbiology.org.
Nitin S
0000-0001-9157-5974
NS
Baliga
D016969:Desulfovibrio vulgaris / Q000235:genetics / Q000254:growth & development*; D019020:Directed Molecular Evolution; D020869:Gene Expression Profiling; D017017:Methanococcus / Q000235:genetics / Q000254:growth & development*; D010084:Oxidation-Reduction; D010641:Phenotype; D040901:Proteomics; D017423:Sequence Analysis, RNA; D059010:Single-Cell Analysis; D013431:Sulfates / Q000378:metabolism; D049490:Systems Biology / Q000379:methods*
D013431:Sulfates
fluctuating resource environment; microbial population collapse; regulation; resilience; syntrophy