Open AccessMechanism for microbial population collapse in a fluctuating resource environment
Author(s) -
Turkarslan Serdar,
Raman Arjun V,
Thompson Anne W,
Arens Christina E,
Gillespie Mark A,
Netzer Frederick,
Hillesland Kristina L,
Stolyar Sergey,
López García de Lomana Adrian,
Reiss David J,
GormanLewis Drew,
Zane Grant M,
Ranish Jeffrey A,
Wall Judy D,
Stahl David A,
Baliga Nitin S
Publication year - 2017
Publication title -
molecular systems biology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 8.523
H-Index - 148
ISSN - 1744-4292
DOI - 10.15252/msb.20167058
Subject(s) - biology , transcriptome , population , mechanism (biology) , genetics , computational biology , gene , gene expression , philosophy , epistemology , demography , sociology
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.