Expansion of nickel binding- and histidine-rich proteins during gastric adaptation of Helicobacter species

Autor: Frédéric Fischer, Egor Vorontsov, Evelyne Turlin, Christian Malosse, Camille Garcia, David L Tabb, Julia Chamot-Rooke, Riccardo Percudani, Daniel Vinella, Hilde De Reuse
Přispěvatelé: Pathogenèse de Helicobacter / Helicobacter Pathogenesis, Université Paris Cité (UPCité)-Microbiologie Intégrative et Moléculaire (UMR6047), Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Spectrométrie de Masse pour la Biologie – Mass Spectrometry for Biology (UTechS MSBio), Institut Pasteur [Paris] (IP)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Università degli studi di Parma = University of Parma (UNIPR), This study was funded by a Projet transversal de Recherche PTR#73-17 of the Institut Pasteur to the Unité Pathogenèse de Helicobacter. This work of the Interdisciplinary Thematic Institute IMCBio, as part of the ITI 2021-2028 program of the University of Strasbourg, CNRS and Inserm, was supported by IdEx Unistra [ANR (agence nationale de la recherche)-10-IDEX-0002], and by SFRI-STRAT'US project (ANR 20-SFRI-0012) and EUR IMCBio (ANR-17-EURE-0023) under the framework of the French Investments for the Future Program. This work has also been supported by the European EPIC-XS project number 823839, funded by the Horizon 2020 program of the European Union., ANR-20-SFRI-0012,STRAT'US,Façonner les talents en formation et en recherche à l'Université de Strasbourg(2020), ANR-17-EURE-0023,IMCBio,Integrative Molecular and Cellular Biology(2017), European Project: 823839,H2020-INFRAIA-2018-1,EPIC-XS(2019)
Jazyk: angličtina
Rok vydání: 2022
Předmět:
Zdroj: Metallomics
Metallomics, 2022, 14 (9), ⟨10.1093/mtomcs/mfac060⟩
ISSN: 1756-5901
1756-591X
DOI: 10.1093/mtomcs/mfac060⟩
Popis: Acquisition and homeostasis of essential metals during host colonization by bacterial pathogens rely on metal uptake, trafficking, and storage proteins. How these factors have evolved within bacterial pathogens is poorly defined. Urease, a nickel enzyme, is essential for Helicobacter pylori to colonize the acidic stomach. Our previous data suggest that acquisition of nickel transporters and a histidine-rich protein (HRP) involved in nickel storage in H. pylori and gastric Helicobacter spp. have been essential evolutionary events for gastric colonization. Using bioinformatics, proteomics, and phylogenetics, we extended this analysis to determine how evolution has framed the repertoire of HRPs among 39 Epsilonproteobacteria; 18 gastric and 11 non-gastric enterohepatic (EH) Helicobacter spp., as well as 10 other Epsilonproteobacteria. We identified a total of 213 HRPs distributed in 22 protein families named orthologous groups (OGs) with His-rich domains, including 15 newly described OGs. Gastric Helicobacter spp. are enriched in HRPs (7.7 ± 1.9 HRPs/strain) as compared to EH Helicobacter spp. (1.9 ± 1.0 HRPs/strain) with a particular prevalence of HRPs with C-terminal histidine-rich domains in gastric species. The expression and nickel-binding capacity of several HRPs was validated in five gastric Helicobacter spp. We established the evolutionary history of new HRP families, such as the periplasmic HP0721-like proteins and the HugZ-type heme oxygenases. The expansion of histidine-rich extensions in gastric Helicobacter spp. proteins is intriguing but can tentatively be associated with the presence of the urease nickel enzyme. We conclude that this HRP expansion is associated with unique properties of organisms that rely on large intracellular nickel amounts for their survival.
Databáze: OpenAIRE
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