Mechanism for microbial population collapse in a fluctuating resource environment
Ontology highlight
ABSTRACT:
INSTRUMENT(S): LTQ Orbitrap Elite
ORGANISM(S): Methanococcus Maripaludis S2 (ncbitaxon:267377) Desulfovibrio Vulgaris Str. Hildenborough (ncbitaxon:882)
SUBMITTER: Jeff Ranish, Nitin Baliga
PROVIDER: MSV000080363 | MassIVE | Mon Nov 28 18:05:00 GMT 2016
SECONDARY ACCESSION(S): PXD005456
REPOSITORIES: MassIVE
Similar Datasets
Project description:Managing tradeoffs through gene regulation is believed to maintain resilience of a microbial community in a fluctuating resource environment. To investigate this hypothesis we imposed a fluctuating environment that required the sulfate-reducing generalist Desulfovibrio vulgaris to manage tradeoffs associated with 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. Most cultures collapsed within 3-7 shifts with only a few collapsing later. 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. The microbial community collapse was rescued by a single regulatory mutation that could then potentially serve as a stepping stone for further adaptive evolution in a variable resource environment. Co-culture strains of M. maripaludis wild type and either wild type or DVU0744::Tn5 mutant of D. vulgaris strains were grown anaerobically in replicates. Samples were transitioned between syntrophic and sulfate respiratory growth conditions at early log phases.
2016-03-10 | E-GEOD-79022 | biostudies-arrayexpress
Project description:Managing tradeoffs through gene regulation is believed to maintain resilience of a microbial community in a fluctuating resource environment. To investigate this hypothesis we imposed a fluctuating environment that required the sulfate-reducing generalist Desulfovibrio vulgaris to manage tradeoffs associated with 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. Most cultures collapsed within 3-7 shifts with only a few collapsing later. 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. The microbial community collapse was rescued by a single regulatory mutation that could then potentially serve as a stepping stone for further adaptive evolution in a variable resource environment.
2016-03-10 | GSE79022 | GEO
Project description:diDO-IPTL proteomics data of Desulfovibrio vulgaris Hildenborough wild type and two DsrC point mutants (IPFG07 & IPFG09) under sulfate-reducing (respiration) and fermentative growth (late-exponential phase)
2022-10-27 | MSV000090596 | MassIVE
Project description:Managing tradeoffs through gene regulation is believed to be critical for the success of a generalist in a fluctuating resource environment. To investigate this hypothesis in depth, we imposed a fluctuating environment that required a representative community of the sulfate-reducing generalist Desulfovibrio vulgaris to manage tradeoffs associated with 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. Counterintuitively, the community rapidly collapsed and went extinct because extensive gene regulation during shifts drove precipitous decline in intracellular abundance of essential transcripts and proteins. We demonstrate that extensive gene regulation can be catastrophic for a generalist when resources fluctuate rapidly, and that the extinction phenomenon can be prevented by a single regulatory mutation that could then potentially serve as a stepping stone for further adaptive evolution in a variable resource environment. Two strains were profiled at early and mid-log phase of growth during Sulfate Respiration and Syntrophy, and after transition between them. 2 biological replicates, 24 samples
2015-09-17 | E-GEOD-73105 | biostudies-arrayexpress
Project description:Managing tradeoffs through gene regulation is believed to be critical for the success of a generalist in a fluctuating resource environment. To investigate this hypothesis in depth, we imposed a fluctuating environment that required a representative community of the sulfate-reducing generalist Desulfovibrio vulgaris to manage tradeoffs associated with 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. Counterintuitively, the community rapidly collapsed and went extinct because extensive gene regulation during shifts drove precipitous decline in intracellular abundance of essential transcripts and proteins. We demonstrate that extensive gene regulation can be catastrophic for a generalist when resources fluctuate rapidly, and that the extinction phenomenon can be prevented by a single regulatory mutation that could then potentially serve as a stepping stone for further adaptive evolution in a variable resource environment.
2015-09-17 | GSE73105 | GEO
Project description:Desulfovibrio vulgaris Hildenborough is a gram-negative anaerobic bacterium belonging to the sulfate-reducing bacteria, a group of microbes that can perform dissimilatory sulfate reduction coupled to the oxidation of various substrates as carbon and energy sources. In the absence of sulfate, they can also ferment organic acids in syntrophy with methanogens. They exhibit high metabolic diversity switching from one energy mode to another depending on nutrients availability in the environments. Hence, they play a central role in shaping ecosystems. Despite, intensive efforts to study D. vulgaris energy metabolism at the genomic, biochemical and ecological level, bioenergetics in this microorganism remains far from being fully understood. Alternatively, few metabolic models were also proposed to explain D. vulgaris bioenergetics. However, they appeared to be not easily adaptable to various environmental conditions. To lift off these limitations, here we constructed a new transparent and robust metabolic model of D. vulgaris bioenergetics by combining whole-cell proteomic analysis with modeling approaches (Flux Balance Analysis). The iDvu71 model showed over 0.95 correlation with experimental data. Further simulations allowed a detailed description of D. vulgaris metabolism in various conditions of growth. Altogether, the simulations run in this study highlighted the sulfate-to-lactate consumption ratio as a pivotal factor in D. vulgaris energy metabolism. In particular, the impact on the hydrogen/formate balance and biomass synthesis is discussed. Overall, this study provides a novel insight into D. vulgaris metabolic flexibility.
2024-02-01 | PXD046638 | Pride
Project description:The sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough possesses four periplasmic hydrogenases to facilitate the oxidation of molecular hydrogen. These include an [Fe], a [NiFeSe] and two [NiFe] hydrogenases encoded by the hyd, hys, hyn1 and hyn2 genes, respectively. In order to understand their cellular functions the expression levels of these hydrogenases, along with the growth rate analysis of mutant strains, was determined during growth on defined media under 3 different conditions. These conditions incuded lactate or hydrogen at either 5% or 50% (vol/vol) used as the sole electron donor for sulfate reduction. Keywords: Electron donor change
2007-07-02 | GSE8137 | GEO
Project description:The synthetic microbial community used in this study was composed of the major functional guilds (cellulolytic fermenter, sulfate reducer, hydrogenotrophic methanogen and acetoclastic methanogen) that mediate the anaerobic conversion of cellulosic biomass to CH4 and CO2 in wetland soils. The choice of a facultative sulfate-reducing bacterium (Desulfovibrio vulgaris Hildenborough) introduced metabolic versatility and enabled investigations into the community response to sulfate intrusion. The growth status of these multi-species cultures was measured over a week by daily analysis of substrate consumption and product accumulation. The quad-cultures were analyzed with metaproteomics at the end of experiment to characterize the community structure and metabolic activities.
2023-02-17 | PXD035759 | Pride
Project description:Purpose: Free nitrous acid (FNA) has recently been demonstrated as an antimicrobial agent to a range of microorganisms. However, its antimicrobial mechanism is largely unknown. For this study Desulfovibrio vulgaris Hildenborough was selected to gain a systematic understanding of the antimicrobial mechanism of FNA. Methods: D. vulgaris was grown under anaerobic denitrifying conditions and when FNA was added (4 μg-N/L) growth temporarily stopped. From cultures with and without added FNA, RNA was extracted and the abundance of gene transcripts was detected by sequencing. Transcripts exhibiting â¥1 or â¤-1 fold abundance change in the presence of FNA were designated as differentially expressed. Results:The results imply that FNA exerted multiple antimicrobial effects. Growth of the culture was inhibited by FNA and significant proportions of the cells were killed during the exposure. Respiration by sulfate reduction and lactate oxidation was shut down along with ATP production when exposed to FNA. Correspondingly, decreased transcript levels of genes involved in these metabolic pathways were detected. Detoxification of FNA was evident by nitrite reduction and the genes coding both nitrite reductase (NrfA) and hydroxylamine reductase were highly up regulated. During the FNA induced energy depleted state, there was evidence that D. vulgaris lowered both ribosome activity and protein production. Conditions within the cells were more oxidizing and genes coding for proteins providing resistance to oxidative stress were up regulated. Culture thiol levels increased during the exposure, suggesting that FNA had caused protein structures to alter. Furthermore, genes for motility were up regulated possibly as an attempt to avoid FNA stress. These findings provide new insight for understanding the response of D. vulgaris to FNA exposure. Conclusion: In this study, we performed genome-wide high throughput RNA sequencing (RNA-Seq) analysis on D. vulgaris in the absence and presence of a bacteriostatic-level of FNA (4 μg-N/L). By combining the global activated/suppressed gene profiles and detected physiological responses, we detected the microbial response to FNA exposure and revealed potential antimicrobial mechanisms of FNA on this prevalent model sulfate reducing bacteria. mRNA profiles of D. vulgaris Hildenborough towards FNA stress were generated by next generation sequencing in triplicate via Illumina 2000.
2016-07-01 | E-GEOD-78834 | biostudies-arrayexpress
Project description:In order to obtain a global view of energy metabolism pathways of the sulfate-reducer Desulfovibrio vulgaris Hildenborough and the proteins involved therein whole-genome microarrays were used to compare the transcriptional response of cells grown with hydrogen/sulfate, pyruvate/sulfate, lactate/thiosulfate, and pyruvate with limiting sulfate, relative to growth in standard lactate/sulfate condition. Growth with hydrogen/sulfate showed the largest number of differently expressed genes and the largest changes in expression levels. The most up-regulated energy metabolism genes were those coding for the periplasmic [NiFeSe] hydrogenase, followed by the Ech hydrogenase, and the most down-regulated were genes coding for the Coo hydrogenase. The results point to the involvement of formate cycling and the ethanol pathway during growth on hydrogen, whereas there is evidence for CO cycling during growth on lactate and pyruvate, but not on H2. Growth with thiosulfate showed the hallmarks of a reduced energy status of the cells with down regulation of the ATP synthase and the Qmo and Dsr complexes., whereas growth with pyruvate showed the smallest differences but an increased role for the Ech hydrogenase.that in this case functions in reverse from the case of growth with H2. The multiple periplasmic hydrogenases and formate dehydrogenases, do not display the same regulation pattern showing that their metabolic roles are not totally interchangeable. This result together with the observation that several genes coding for proteins that have not been biochemically characterised were considerably affected in this study, reveals a more complex energy metabolism than previously considered and provides guidance for further studies. Keywords: Growth protocol Desulfovibrio vulgaris from our laboratory culture collection was cultured at 37°C with pyruvate as the only substrate (without sulfate as the electron acceptor) to mid-log phase. Cultures were also cultivated similarly in Lactate-Sulfate medium to mid-log phase. Gene expression profiles of cultures grown under pyruvate fermentation were compared with those of the cultures grown via sulfate reduction. Total RNA was harvested from four replicate cultures for microarray analysis. RNA extraction, purification, and labeling were performed independently on each cell sample.Two samples of each total RNA preparation were labeled, one with Cy3-dUTP and another with Cy5-dUTP for microarray hybridization.
2008-05-31 | E-GEOD-8015 | biostudies-arrayexpress