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Metabolic robustness to growth temperature of a cold adapted bacterium

Christopher Riccardi, Marzia Calvanese, Veronica Ghini, Tania Alonso-Vásquez, Elena Perrin, Paola Turano, Giorgio Giurato, Alessandro Weisz, Ermenegilda Parrilli, Maria Luisa Tutino, View ORCID ProfileMarco Fondi
doi: https://doi.org/10.1101/2022.10.25.513664
Christopher Riccardi
1Department of Biology, University of Florence, Via Madonna del Piano 6, 50019 Sesto F.no, Florence, Italy
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Marzia Calvanese
2Dipartimento di Scienze Chimiche, University of Naples, edificio MB Via Cintia Monte S. Angelo 80126 Napoli - Italy
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Veronica Ghini
3Center of Magnetic Resonance (CERM), University of Florence, Italy
4Consorzio Interuniversitario Risonanze Magnetiche di Metallo Proteine (CIRMMP), Florence, Italy
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Tania Alonso-Vásquez
1Department of Biology, University of Florence, Via Madonna del Piano 6, 50019 Sesto F.no, Florence, Italy
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Elena Perrin
1Department of Biology, University of Florence, Via Madonna del Piano 6, 50019 Sesto F.no, Florence, Italy
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Paola Turano
3Center of Magnetic Resonance (CERM), University of Florence, Italy
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Giorgio Giurato
5Department of Medicine, Surgery and Dentistry ‘Scuola Medica Salernitana’, University of Salerno, Via S. Allende, 84081 Baronissi, Italy
6Genome Research Center for Health - GRGS, Campus di Medicina, Via S. Allende, 84081 Baronissi, Italy
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Alessandro Weisz
5Department of Medicine, Surgery and Dentistry ‘Scuola Medica Salernitana’, University of Salerno, Via S. Allende, 84081 Baronissi, Italy
6Genome Research Center for Health - GRGS, Campus di Medicina, Via S. Allende, 84081 Baronissi, Italy
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Ermenegilda Parrilli
2Dipartimento di Scienze Chimiche, University of Naples, edificio MB Via Cintia Monte S. Angelo 80126 Napoli - Italy
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Maria Luisa Tutino
2Dipartimento di Scienze Chimiche, University of Naples, edificio MB Via Cintia Monte S. Angelo 80126 Napoli - Italy
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Marco Fondi
1Department of Biology, University of Florence, Via Madonna del Piano 6, 50019 Sesto F.no, Florence, Italy
7Centro interdipartimentale per lo Studio delle Dinamiche Complesse (CSDC), University of Florence, Italy
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  • ORCID record for Marco Fondi
  • For correspondence: marco.fondi@unifi.it
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Abstract

Microbial communities experience continuous environmental changes, among which temperature fluctuations are arguably the most impacting. This is particularly important considering the ongoing global warming but also in the “simpler” context of seasonal variability of sea-surface temperature. Understanding how microorganisms react at the cellular level can improve our understanding of possible adaptations of microbial communities to a changing environment. In this work, we investigated which are the mechanisms through which metabolic homeostasis is maintained in a cold-adapted bacterium during growth at temperatures that differ widely (15 and 0°C). We have quantified its intracellular and extracellular central metabolomes together with changes occurring at the transcriptomic level in the same growth conditions. This information was then used to contextualize a genome-scale metabolic reconstruction and to provide a systemic understanding of cellular adaptation to growth at two different temperatures. Our findings indicate a strong metabolic robustness at the level of the main central metabolites, counteracted by a relatively deep transcriptomic reprogramming that includes changes in gene expression of hundreds of metabolic genes. We interpret this as a transcriptomic buffering of cellular metabolism, able to produce overlapping metabolic phenotypes despite the wide temperature gap. Moreover, we show that metabolic adaptation seems to be mostly played at the level of few key intermediates (e.g. phosphoenolpyruvate) and in the cross-talk between the main central metabolic pathways. Overall, our findings reveal a complex interplay at gene expression level that contributes to the robustness/resilience of core metabolism, also promoting the leveraging of state-of-the-art multi-disciplinary approaches to fully comprehend molecular adaptations to environmental fluctuations.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/combogenomics/MetRob015

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted October 26, 2022.
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Metabolic robustness to growth temperature of a cold adapted bacterium
Christopher Riccardi, Marzia Calvanese, Veronica Ghini, Tania Alonso-Vásquez, Elena Perrin, Paola Turano, Giorgio Giurato, Alessandro Weisz, Ermenegilda Parrilli, Maria Luisa Tutino, Marco Fondi
bioRxiv 2022.10.25.513664; doi: https://doi.org/10.1101/2022.10.25.513664
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Metabolic robustness to growth temperature of a cold adapted bacterium
Christopher Riccardi, Marzia Calvanese, Veronica Ghini, Tania Alonso-Vásquez, Elena Perrin, Paola Turano, Giorgio Giurato, Alessandro Weisz, Ermenegilda Parrilli, Maria Luisa Tutino, Marco Fondi
bioRxiv 2022.10.25.513664; doi: https://doi.org/10.1101/2022.10.25.513664

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