Extracellular metabolite dynamics and temporal organization of metabolic function in E. coli

Robert, Martin; Murray, Douglas B.; Honma, Masayuki; Nakahigashi, Kenji; Soga, Tomoyoshi; Tomita, Masaru

doi:10.1109/iccme.2012.6275650

Cited by 4 publications

(3 citation statements)

References 23 publications

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“…Metabolic responses are generally fast, making it difficult to analyze their dynamics and understand the specific mechanisms underlying self-organization in a given species. However, some biological systems will spontaneously develop stable oscillations in continuous culture at high cell density (4)(5)(6)(7)(8)(9)(10)(11). These oscillating cultures offer an opportunity to understand fundamental principles of metabolic regulation and what limits metabolism.…”

mentioning

confidence: 99%

Redox controls metabolic robustness in the gas-fermenting acetogenClostridium autoethanogenum

Mahamkali

Valgepea

Lemgruber

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

111

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Living biological systems display a fascinating ability to self-organize their metabolism. This ability ultimately determines the metabolic robustness that is fundamental to controlling cellular behavior. However, fluctuations in metabolism can affect cellular homeostasis through transient oscillations. For example, yeast cultures exhibit rhythmic oscillatory behavior in high cell-density continuous cultures. Oscillatory behavior provides a unique opportunity for quantitating the robustness of metabolism, as cells respond to changes by inherently compromising metabolic efficiency. Here, we quantify the limits of metabolic robustness in self-oscillating autotrophic continuous cultures of the gas-fermenting acetogenClostridium autoethanogenum. Online gas analysis and high-resolution temporal metabolomics showed oscillations in gas uptake rates and extracellular byproducts synchronized with biomass levels. The data show initial growth on CO, followed by growth on CO and H2. Growth on CO and H2results in an accelerated growth phase, after which a downcycle is observed in synchrony with a loss in H2uptake. Intriguingly, oscillations are not linked to translational control, as no differences were observed in protein expression during oscillations. Intracellular metabolomics analysis revealed decreasing levels of redox ratios in synchrony with the cycles. We then developed a thermodynamic metabolic flux analysis model to investigate whether regulation in acetogens is controlled at the thermodynamic level. We used endo- and exo-metabolomics data to show that the thermodynamic driving force of critical reactions collapsed as H2uptake is lost. The oscillations are coordinated with redox. The data indicate that metabolic oscillations in acetogen gas fermentation are controlled at the thermodynamic level.

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mentioning

confidence: 99%

Redox controls metabolic robustness in the gas-fermenting acetogenClostridium autoethanogenum

Mahamkali

Valgepea

Lemgruber

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

111

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“…While the exact mechanisms of synchronization have not been clarified, the cellular redox state as well as H 2 S and acetaldehyde levels have been found to be important [12][13][14]. In E. coli, valine and other metabolite exchanges might be responsible for similar synchronization events [15]. Such results suggest that most, if not all, cellular components oscillate, claims supported by other studies [16] and in other systems [17].…”

Section: 3mentioning

confidence: 71%

A Broader Perspective About Organization and Coherence in Biological Systems

Robert

2013

Proceedings of the European Conference on Complex Systems 2012

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The implications of large-scale coherence in biological systems and possible links to quantum theory are only beginning to be explored. Whether quantum-like coherent phenomena are relevant, or even possible at all, at the high temperatures of biological systems remains unsettled. Here, we present a broader perspective on biological organization and how quantum-like dynamics and coherence might shape the very fabric from which complex biological systems are organized. Regardless of its exact nature, a unique form of coherence seems apparent at multiple scales in biology and its better characterization may have broad consequences for the understanding of living organisms as complex systems.

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“…Nevertheless, observations of oscillation in continuous cultivations of microbes are not uncommon [4]. Metabolic oscillations in continuous culture are reported for many bacteria, including Escherichia coli [5][6][7], Zymomonas mobilis [8] and Klebsiella pneumoniae [9,10] as well as the yeast Saccharomyces cerevisiae [11][12][13][14][15][16].…”

Section: Introductionmentioning

confidence: 99%

Metabolic Oscillation Phenomena in Clostridia Species—A Review

Tyszak,

Rehmann

2024

Fermentation

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Clostridia are interesting candidates for biotechnological applications due to their diverse and unique metabolic abilities. Particularly in continuous fermentation processes, productivity-decreasing metabolic oscillations have been reported in many species. The resulting process instability and reduced productivity can be a serious hurdle for the development of industrially feasible processes. This review highlights the current state of knowledge about oscillatory metabolic phenomena in Clostridia, including the mechanisms, assumed and proven, behind those oscillations and methods to mitigate the phenomena if applicable. The nature of observed metabolic oscillations in Clostridia is diverse, including a wide range of periods of oscillation and different parameters in which the oscillation is observed. Some phenomena remain to be investigated further, while others are already well understood. However, knowledge of mechanisms is a very valuable asset in overcoming the metabolic oscillation to create a stable process.

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Extracellular metabolite dynamics and temporal organization of metabolic function in E. coli

Cited by 4 publications

References 23 publications

Redox controls metabolic robustness in the gas-fermenting acetogenClostridium autoethanogenum

Redox controls metabolic robustness in the gas-fermenting acetogenClostridium autoethanogenum

A Broader Perspective About Organization and Coherence in Biological Systems

Metabolic Oscillation Phenomena in Clostridia Species—A Review

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