Cargando…

The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems

Pectobacterium versatile (formerly P. carotovorum) is a recently defined species of soft rot enterobacteria capable of infecting many plant hosts and damaging different tissues. Complex transcriptional regulation of virulence properties can be expected for such a versatile pathogen. However, the rel...

Descripción completa

Detalles Bibliográficos
Autores principales: Kravchenko, Uljana, Gogoleva, Natalia, Kalubaka, Nastassia, Kruk, Alla, Diubo, Yuliya, Gogolev, Yuri, Nikolaichik, Yevgeny
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7843439/
https://www.ncbi.nlm.nih.gov/pubmed/33519782
http://dx.doi.org/10.3389/fmicb.2020.621391
_version_ 1783644143161966592
author Kravchenko, Uljana
Gogoleva, Natalia
Kalubaka, Nastassia
Kruk, Alla
Diubo, Yuliya
Gogolev, Yuri
Nikolaichik, Yevgeny
author_facet Kravchenko, Uljana
Gogoleva, Natalia
Kalubaka, Nastassia
Kruk, Alla
Diubo, Yuliya
Gogolev, Yuri
Nikolaichik, Yevgeny
author_sort Kravchenko, Uljana
collection PubMed
description Pectobacterium versatile (formerly P. carotovorum) is a recently defined species of soft rot enterobacteria capable of infecting many plant hosts and damaging different tissues. Complex transcriptional regulation of virulence properties can be expected for such a versatile pathogen. However, the relevant information is available only for related species and is rather limited. The PhoPQ two-component system, originally described in pectobacteria as PehRS, was previously shown to regulate a single gene, pehA. Using an insertional phoP mutant of Pectobacterium versatile (earlier—P. carotovorum), we demonstrate that PhoP regulates at least 115 genes with a majority of them specific for pectobacteria. The functions performed by PhoP-controlled genes include degradation, transport and metabolism of plant-derived carbon sources (polygalacturonate, arabinose-containing polysaccharides and citrate), modification of bacterial cell envelope and stress resistance. We also demonstrated PhoP involvement in establishing the order of plant cell wall decomposition and utilisation of the corresponding breakdown products. Based on experimental data and in silico analysis, we defined a PhoP binding site motif and provided proof for its universality in enteric bacteria. Scanning P. versatile genome for the locations of this motif suggested a much larger PhoP regulon enriched with the genes important for a plant pathogen, which makes PhoP a global virulence regulator. Potential PhoP targets include many regulatory genes and PhoP control over one of them, expI, was confirmed experimentally, highlighting the link between the PhoPQ two-component and quorum sensing systems. High concentrations of calcium and magnesium ions were found to abolish the PhoPQ-dependent transcription activation but did not relieve repression. Reduced PhoP expression and minimisation of PhoP dependence of regulon members’ expression in P. versatile cells isolated from potato tuber tissues suggest that PhoPQ system is a key switch of expression levels of multiple virulence-related genes fine-tuned to control the development of P. versatile-host plant pathosystem.
format Online
Article
Text
id pubmed-7843439
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-78434392021-01-30 The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems Kravchenko, Uljana Gogoleva, Natalia Kalubaka, Nastassia Kruk, Alla Diubo, Yuliya Gogolev, Yuri Nikolaichik, Yevgeny Front Microbiol Microbiology Pectobacterium versatile (formerly P. carotovorum) is a recently defined species of soft rot enterobacteria capable of infecting many plant hosts and damaging different tissues. Complex transcriptional regulation of virulence properties can be expected for such a versatile pathogen. However, the relevant information is available only for related species and is rather limited. The PhoPQ two-component system, originally described in pectobacteria as PehRS, was previously shown to regulate a single gene, pehA. Using an insertional phoP mutant of Pectobacterium versatile (earlier—P. carotovorum), we demonstrate that PhoP regulates at least 115 genes with a majority of them specific for pectobacteria. The functions performed by PhoP-controlled genes include degradation, transport and metabolism of plant-derived carbon sources (polygalacturonate, arabinose-containing polysaccharides and citrate), modification of bacterial cell envelope and stress resistance. We also demonstrated PhoP involvement in establishing the order of plant cell wall decomposition and utilisation of the corresponding breakdown products. Based on experimental data and in silico analysis, we defined a PhoP binding site motif and provided proof for its universality in enteric bacteria. Scanning P. versatile genome for the locations of this motif suggested a much larger PhoP regulon enriched with the genes important for a plant pathogen, which makes PhoP a global virulence regulator. Potential PhoP targets include many regulatory genes and PhoP control over one of them, expI, was confirmed experimentally, highlighting the link between the PhoPQ two-component and quorum sensing systems. High concentrations of calcium and magnesium ions were found to abolish the PhoPQ-dependent transcription activation but did not relieve repression. Reduced PhoP expression and minimisation of PhoP dependence of regulon members’ expression in P. versatile cells isolated from potato tuber tissues suggest that PhoPQ system is a key switch of expression levels of multiple virulence-related genes fine-tuned to control the development of P. versatile-host plant pathosystem. Frontiers Media S.A. 2021-01-15 /pmc/articles/PMC7843439/ /pubmed/33519782 http://dx.doi.org/10.3389/fmicb.2020.621391 Text en Copyright © 2021 Kravchenko, Gogoleva, Kalubaka, Kruk, Diubo, Gogolev and Nikolaichik. http://creativecommons.org/licenses/by/4.0/ 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) and the copyright owner(s) 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.
spellingShingle Microbiology
Kravchenko, Uljana
Gogoleva, Natalia
Kalubaka, Nastassia
Kruk, Alla
Diubo, Yuliya
Gogolev, Yuri
Nikolaichik, Yevgeny
The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems
title The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems
title_full The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems
title_fullStr The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems
title_full_unstemmed The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems
title_short The PhoPQ Two-Component System Is the Major Regulator of Cell Surface Properties, Stress Responses and Plant-Derived Substrate Utilisation During Development of Pectobacterium versatile-Host Plant Pathosystems
title_sort phopq two-component system is the major regulator of cell surface properties, stress responses and plant-derived substrate utilisation during development of pectobacterium versatile-host plant pathosystems
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7843439/
https://www.ncbi.nlm.nih.gov/pubmed/33519782
http://dx.doi.org/10.3389/fmicb.2020.621391
work_keys_str_mv AT kravchenkouljana thephopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT gogolevanatalia thephopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT kalubakanastassia thephopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT krukalla thephopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT diuboyuliya thephopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT gogolevyuri thephopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT nikolaichikyevgeny thephopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT kravchenkouljana phopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT gogolevanatalia phopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT kalubakanastassia phopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT krukalla phopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT diuboyuliya phopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT gogolevyuri phopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems
AT nikolaichikyevgeny phopqtwocomponentsystemisthemajorregulatorofcellsurfacepropertiesstressresponsesandplantderivedsubstrateutilisationduringdevelopmentofpectobacteriumversatilehostplantpathosystems