Bacterial adaptation to cold: Conservation of a short J-domain co-chaperone and its protein partners in environmental proteobacteria

Lana Weber, Atar Gilat, Nathanael Maillot, Deborah Byrne, Pascal Arnoux, Marie-Therese Giudici-Orticoni, Vincent Mejean, Marianne Ilbert, Olivier Genest, Rina Rosenzweig, Sebastien Dementin*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

1 Citation (Scopus)

Abstract

Bacterial genomes are a huge reservoir of genes encoding J-domain protein co-chaperones that recruit the molecular chaperone DnaK to assist protein substrates involved in survival, adaptation, or fitness. The atc operon of the aquatic mesophilic bacterium Shewanella oneidensis encodes the proteins AtcJ, AtcA, AtcB, and AtcC, and all of them, except AtcA, are required for growth at low temperatures. AtcJ is a short J-domain protein that interacts with DnaK, but also with AtcC through its 21 amino acid C-terminal domain. This interaction network is critical for cold growth. Here, we show that AtcJ represents a subfamily of short J-domain proteins that (i) are found in several environmental, mostly aquatic, ss- or.-proteobacteria and (ii) contain a conserved PX7W motif in their C-terminal extension. Using a combination of NMR, biochemical and genetic approaches, we show that the hydrophobic nature of the tryptophan of the S. oneidensis AtcJ PX7W motif determines the strong AtcJ-AtcC interaction essential for cold growth. The AtcJ homologues are encoded by operons containing at least the S. oneidensis atcA, atcB, and atcC homologues. These findings suggest a conserved network of DnaK and Atc proteins necessary for low-temperature growth and, given the variation in the atc operons, possibly for other biological functions.
Original languageEnglish
Pages (from-to)2447-2464
Number of pages18
JournalEnvironmental Microbiology
Volume25
Issue number11
Early online date7 Aug 2023
DOIs
Publication statusPublished - Nov 2023

Funding

We thank the members of the Bip1 team for their help and suggestions during completion of this work. We thank Mathieu Rebeaud for helpful discussions related to the phylogeny of Atc proteins. We also thank Amane Kriach and Caroline Stemmler for their help on this project. The authors are thankful for the funding from Agence Nationale de la Recherche (ANR-16-CE11-0002-01, and ANR-19-CE44-0018), Aix-Marseille Université and the Centre National de la Recherche Scientifique. Author contributions - Lana Weber: Formal analysis (equal); investigation (equal); methodology (equal). Atar Gilat: Formal analysis (equal); investigation (equal); methodology (equal). Nathanael Maillot: Formal analysis (equal); investigation (equal); methodology (equal). Deborah Byrne: Formal analysis (equal); investigation (equal); methodology (equal); validation (equal). Pascal Arnoux: Conceptualization (equal); writing – review and editing (equal). Marie-Thérèse Giudici-Orticoni: Formal analysis (equal); writing – review and editing (equal). Vincent Méjean: Conceptualization (equal); formal analysis (equal); writing – review and editing (equal). Marianne Ilbert: Formal analysis (equal); investigation (equal); methodology (equal); validation (equal); writing – review and editing (equal). Olivier Genest: Conceptualization (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – review and editing (equal). Rina Rosenzweig: Conceptualization (equal); formal analysis (equal); investigation (equal); methodology (equal); validation (equal); writing – review and editing (equal). Sébastien Dementin: Conceptualization (equal); formal analysis (equal); investigation (equal); methodology (equal); project administration (equal); validation (equal); writing – original draft (equal); writing – review and editing (equal).

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