Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion

ABSTRACT Many plant-pathogenic bacteria of considerable economic importance rely on type III secretion systems (T3SSs) of the Hrc-Hrp 1 family to subvert their plant hosts. T3SS gene expression is regulated through the HrpG and HrpV proteins, while secretion is controlled by the gatekeeper HrpJ. A l...

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Autores principales: Spyridoula N. Charova, Anastasia D. Gazi, Efstratios Mylonas, Charalambos Pozidis, Blanca Sabarit, Dimitrios Anagnostou, Konstantina Psatha, Michalis Aivaliotis, Carmen R. Beuzon, Nickolas J. Panopoulos, Michael Kokkinidis
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:bc30bf14e07c48469230d4ed12b927562021-11-15T16:00:15ZMigration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion10.1128/mBio.01096-182150-7511https://doaj.org/article/bc30bf14e07c48469230d4ed12b927562018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01096-18https://doaj.org/toc/2150-7511ABSTRACT Many plant-pathogenic bacteria of considerable economic importance rely on type III secretion systems (T3SSs) of the Hrc-Hrp 1 family to subvert their plant hosts. T3SS gene expression is regulated through the HrpG and HrpV proteins, while secretion is controlled by the gatekeeper HrpJ. A link between the two mechanisms was so far unknown. Here, we show that a mechanistic coupling exists between the expression and secretion cascades through the direct binding of the HrpG/HrpV heterodimer, acting as a T3SS chaperone, to HrpJ. The ternary complex is docked to the cytoplasmic side of the inner bacterial membrane and orchestrates intermediate substrate secretion, without affecting early substrate secretion. The anchoring of the ternary complex to the membranes potentially keeps HrpG/HrpV away from DNA. In their multiple roles as transcriptional regulators and gatekeeper chaperones, HrpV/HrpG provide along with HrpJ potentially attractive targets for antibacterial strategies. IMPORTANCE On the basis of scientific/economic importance, Pseudomonas syringae and Erwinia amylovora are considered among the top 10 plant-pathogenic bacteria in molecular plant pathology. Both employ type III secretion systems (T3SSs) of the Hrc-Hrp 1 family to subvert their plant hosts. For Hrc-Hrp 1, no functional link was known between the key processes of T3SS gene expression and secretion. Here, we show that a mechanistic coupling exists between expression and secretion cascades, through formation of a ternary complex involving the T3SS proteins HrpG, HrpV, and HrpJ. Our results highlight the functional and structural properties of a hitherto-unknown complex which orchestrates intermediate T3SS substrate secretion and may lead to better pathogen control through novel targets for antibacterial strategies.Spyridoula N. CharovaAnastasia D. GaziEfstratios MylonasCharalambos PozidisBlanca SabaritDimitrios AnagnostouKonstantina PsathaMichalis AivaliotisCarmen R. BeuzonNickolas J. PanopoulosMichael KokkinidisAmerican Society for MicrobiologyarticleErwinia amylovoraPseudomonas syringae pv. phaseolicolatype III secretion system (T3SS)gatekeeper complexMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution DOAJ
collection DOAJ
language EN
topic Erwinia amylovora
Pseudomonas syringae pv. phaseolicola
type III secretion system (T3SS)
gatekeeper complex
Microbiology
QR1-502
spellingShingle Erwinia amylovora
Pseudomonas syringae pv. phaseolicola
type III secretion system (T3SS)
gatekeeper complex
Microbiology
QR1-502
Spyridoula N. Charova
Anastasia D. Gazi
Efstratios Mylonas
Charalambos Pozidis
Blanca Sabarit
Dimitrios Anagnostou
Konstantina Psatha
Michalis Aivaliotis
Carmen R. Beuzon
Nickolas J. Panopoulos
Michael Kokkinidis
Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion
description ABSTRACT Many plant-pathogenic bacteria of considerable economic importance rely on type III secretion systems (T3SSs) of the Hrc-Hrp 1 family to subvert their plant hosts. T3SS gene expression is regulated through the HrpG and HrpV proteins, while secretion is controlled by the gatekeeper HrpJ. A link between the two mechanisms was so far unknown. Here, we show that a mechanistic coupling exists between the expression and secretion cascades through the direct binding of the HrpG/HrpV heterodimer, acting as a T3SS chaperone, to HrpJ. The ternary complex is docked to the cytoplasmic side of the inner bacterial membrane and orchestrates intermediate substrate secretion, without affecting early substrate secretion. The anchoring of the ternary complex to the membranes potentially keeps HrpG/HrpV away from DNA. In their multiple roles as transcriptional regulators and gatekeeper chaperones, HrpV/HrpG provide along with HrpJ potentially attractive targets for antibacterial strategies. IMPORTANCE On the basis of scientific/economic importance, Pseudomonas syringae and Erwinia amylovora are considered among the top 10 plant-pathogenic bacteria in molecular plant pathology. Both employ type III secretion systems (T3SSs) of the Hrc-Hrp 1 family to subvert their plant hosts. For Hrc-Hrp 1, no functional link was known between the key processes of T3SS gene expression and secretion. Here, we show that a mechanistic coupling exists between expression and secretion cascades, through formation of a ternary complex involving the T3SS proteins HrpG, HrpV, and HrpJ. Our results highlight the functional and structural properties of a hitherto-unknown complex which orchestrates intermediate T3SS substrate secretion and may lead to better pathogen control through novel targets for antibacterial strategies.
format article
author Spyridoula N. Charova
Anastasia D. Gazi
Efstratios Mylonas
Charalambos Pozidis
Blanca Sabarit
Dimitrios Anagnostou
Konstantina Psatha
Michalis Aivaliotis
Carmen R. Beuzon
Nickolas J. Panopoulos
Michael Kokkinidis
author_facet Spyridoula N. Charova
Anastasia D. Gazi
Efstratios Mylonas
Charalambos Pozidis
Blanca Sabarit
Dimitrios Anagnostou
Konstantina Psatha
Michalis Aivaliotis
Carmen R. Beuzon
Nickolas J. Panopoulos
Michael Kokkinidis
author_sort Spyridoula N. Charova
title Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion
title_short Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion
title_full Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion
title_fullStr Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion
title_full_unstemmed Migration of Type III Secretion System Transcriptional Regulators Links Gene Expression to Secretion
title_sort migration of type iii secretion system transcriptional regulators links gene expression to secretion
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/bc30bf14e07c48469230d4ed12b92756
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