Dataset Information

Mechanism for microbial population collapse in a fluctuating resource environment.

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.

SUBMITTER: Turkarslan S

PROVIDER: S-EPMC5371734 | biostudies-literature | 2017 Mar

REPOSITORIES: biostudies-literature

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Mechanism for microbial population collapse in a fluctuating resource environment.

Turkarslan Serdar S Raman Arjun V AV Thompson Anne W AW Arens Christina E CE Gillespie Mark A MA von Netzer Frederick F Hillesland Kristina L KL Stolyar Sergey S López García de Lomana Adrian A Reiss David J DJ Gorman-Lewis Drew D Zane Grant M GM Ranish Jeffrey A JA Wall Judy D JD Stahl David A DA Baliga Nitin S NS

Molecular systems biology 20170320 3

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 <i>Desulfovibrio vulgaris</i> 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-consumin ...[more]

PMID: 28320772

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Project description:During the 1960s, small quantities of radioactive materials were codisposed with chemical waste at the Little Forest Legacy Site (Sydney, Australia) in 3-meter-deep, unlined trenches. Chemical and microbial analyses, including functional and taxonomic information derived from shotgun metagenomics, were collected across a 6-week period immediately after a prolonged rainfall event to assess the impact of changing water levels upon the microbial ecology and contaminant mobility. Collectively, results demonstrated that oxygen-laden rainwater rapidly altered the redox balance in the trench water, strongly impacting microbial functioning as well as the radiochemistry. Two contaminants of concern, plutonium and americium, were shown to transition from solid-iron-associated species immediately after the initial rainwater pulse to progressively more soluble moieties as reducing conditions were enhanced. Functional metagenomics revealed the potentially important role that the taxonomically diverse microbial community played in this transition. In particular, aerobes dominated in the first day, followed by an increase of facultative anaerobes/denitrifiers at day 4. Toward the mid-end of the sampling period, the functional and taxonomic profiles depicted an anaerobic community distinguished by a higher representation of dissimilatory sulfate reduction and methanogenesis pathways. Our results have important implications to similar near-surface environmental systems in which redox cycling occurs.IMPORTANCE The role of chemical and microbiological factors in mediating the biogeochemistry of groundwaters from trenches used to dispose of radioactive materials during the 1960s is examined in this study. Specifically, chemical and microbial analyses, including functional and taxonomic information derived from shotgun metagenomics, were collected across a 6-week period immediately after a prolonged rainfall event to assess how changing water levels influence microbial ecology and contaminant mobility. Results demonstrate that oxygen-laden rainwater rapidly altered the redox balance in the trench water, strongly impacting microbial functioning as well as the radiochemistry. Two contaminants of concern, plutonium and americium, were shown to transition from solid-iron-associated species immediately after the initial rainwater pulse to progressively more soluble moieties as reducing conditions were enhanced. Functional metagenomics revealed the important role that the taxonomically diverse microbial community played in this transition. Our results have important implications to similar near-surface environmental systems in which redox cycling occurs.

Dataset Information

Mechanism for microbial population collapse in a fluctuating resource environment.

Publications

Mechanism for microbial population collapse in a fluctuating resource environment.

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