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An important role for periplasmic storage in Pseudomonas aeruginosa copper homeostasis revealed by a combined experimental and computational modeling study

Jignesh H. Parmar, Julia Quintana, David Ramírez, Reinhard Laubenbacher, José M. Argüello, Pedro Mendes
doi: https://doi.org/10.1101/301002
Jignesh H. Parmar
1Center for Quantitative Medicine and Department of Cell Biology, University of Connecticut School of Medicine, 263 Farmington Av., Farmington, CT, 06030, USA
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Julia Quintana
2Department of Chemistry and Biochemistry, Worcester Polytechnic Institute, 100 Institute Road, Worcester, MA, 01609, USA
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David Ramírez
2Department of Chemistry and Biochemistry, Worcester Polytechnic Institute, 100 Institute Road, Worcester, MA, 01609, USA
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Reinhard Laubenbacher
1Center for Quantitative Medicine and Department of Cell Biology, University of Connecticut School of Medicine, 263 Farmington Av., Farmington, CT, 06030, USA
3Jackson Laboratory for Genomic Medicine, 10 Discovery Dr., Farmington, CT, 06032, USA
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José M. Argüello
2Department of Chemistry and Biochemistry, Worcester Polytechnic Institute, 100 Institute Road, Worcester, MA, 01609, USA
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Pedro Mendes
1Center for Quantitative Medicine and Department of Cell Biology, University of Connecticut School of Medicine, 263 Farmington Av., Farmington, CT, 06030, USA
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  • For correspondence: pmendes@uchc.edu
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Summary

Biological systems require precise copper homeostasis enabling metallation of cuproproteins while preventing metal toxicity. In bacteria, sensing, transport and storage molecules act in coordination to fulfill these roles. However, there is not yet a kinetic schema explaining the system integration. Here, we report a model emerging from experimental and computational approaches that describes the dynamics of copper distribution in Pseudomonas aeruginosa. Based on copper uptake experiments, a minimal kinetic model describes well the copper distribution in the wild type bacteria but is unable to explain the behavior of the mutant strain lacking CopA1, a key Cu+ efflux ATPase. The model was expanded through an iterative hypothesis-driven approach, arriving to a mechanism that considers the induction of compartmental pools and the parallel function of CopA and Cus efflux systems. Model simulations support the presence of a periplasmic copper storage with a crucial role under dyshomeostasis conditions in P. aeruginosa. Importantly, the model predicts not only the interplay of periplasmic and cytoplasmic pools but also the existence of a threshold in the concentration of external copper beyond which cells lose their ability to control copper levels.

Footnotes

  • ↵* JHP and JQ should be considered joint first author.

  • ↵† RL, JMA and PM should be considered joint senior author.

Copyright 
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 July 13, 2018.
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An important role for periplasmic storage in Pseudomonas aeruginosa copper homeostasis revealed by a combined experimental and computational modeling study
Jignesh H. Parmar, Julia Quintana, David Ramírez, Reinhard Laubenbacher, José M. Argüello, Pedro Mendes
bioRxiv 301002; doi: https://doi.org/10.1101/301002
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An important role for periplasmic storage in Pseudomonas aeruginosa copper homeostasis revealed by a combined experimental and computational modeling study
Jignesh H. Parmar, Julia Quintana, David Ramírez, Reinhard Laubenbacher, José M. Argüello, Pedro Mendes
bioRxiv 301002; doi: https://doi.org/10.1101/301002

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