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ORIGINAL RESEARCH article

Front. Microbiol.
Sec. Biology of Archaea
Volume 15 - 2024 | doi: 10.3389/fmicb.2024.1475385

Impact of nutrient excess on physiology and metabolism of Sulfolobus acidocaldarius

Provisionally accepted
Viktor L. Sedlmayr Viktor L. Sedlmayr 1Diana Széliová Diana Széliová 2Veerke De Kock Veerke De Kock 3Yannick G. Gansemans Yannick G. Gansemans 4*Filip Van Nieuwerburgh Filip Van Nieuwerburgh 5Eveline Peeters Eveline Peeters 3Julian Quehenberger Julian Quehenberger 1Jürgen Zanghellini Jürgen Zanghellini 2Oliver Spadiut Oliver Spadiut 1*
  • 1 Institute of Chemical, Environmental and Bioscience, Vienna University of Technology, Vienna, Vienna, Austria
  • 2 Department of Analytical Chemistry, University of Vienna, Vienna, Vienna, Austria
  • 3 Department of Bioengineering Sciences, Vrije University Brussels, Brussels, Brussels, Belgium
  • 4 Department of Pharmaceutics, Ghent University, Ghent, East Flanders, Belgium
  • 5 Department of Pharmaceutics, Ghent University, Ghent, Belgium

The final, formatted version of the article will be published soon.

    Overflow metabolism is a well-known phenomenon that describes the seemingly wasteful and incomplete substrate oxidation by aerobic cells, such as yeasts, bacteria, and mammalian cells, even when conditions allow for total combustion via respiration. This cellular response, triggered by an excess of C-source, has not yet been investigated in archaea. In this study, we conducted chemostat cultivations to compare the metabolic and physiological states of the thermoacidophilic archaeon Sulfolobus acidocaldarius under three conditions, each with gradually increasing nutrient stress. Our results show that S. acidocaldarius has different capacities for the uptake of the two C-sources, monosodium glutamate and glucose. A saturated tricarboxylic acid cycle at elevated nutrient concentrations affects the cell's ability to deplete its intermediates. This includes deploying additional cataplerotic pathways and the secretion of amino acids, notably valine, glycine, and alanine, while glucose is increasingly metabolized via glycogenesis. We did not observe the secretion of common fermentation products, like organic acids. Transcriptomic analysis indicated an upregulation of genes involved in fatty acid metabolism, suggesting the intracellular conservation of energy. Adapting respiratory enzymes under nutrient stress indicated high metabolic flexibility and robust regulatory mechanisms in this archaeon. This study enhances our fundamental understanding of the metabolism of S. acidocaldarius.

    Keywords: Sulfolobus acidocaldarius, Chemostat cultivation, overflow metabolism, carbon overfeeding, fatty acid metabolism, transcriptome analysis, Archaea, parsimonious flux balance analysis

    Received: 03 Aug 2024; Accepted: 13 Sep 2024.

    Copyright: © 2024 Sedlmayr, Széliová, De Kock, Gansemans, Van Nieuwerburgh, Peeters, Quehenberger, Zanghellini and Spadiut. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

    * Correspondence:
    Yannick G. Gansemans, Department of Pharmaceutics, Ghent University, Ghent, 9000, East Flanders, Belgium
    Oliver Spadiut, Institute of Chemical, Environmental and Bioscience, Vienna University of Technology, Vienna, 1040, Vienna, Austria

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