Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks

International audience Vibrio tapetis causes the brown ring disease in the Japanese clam Ruditapes philippinarum while Vibrio aestuarianus is associated with massive oyster mortalities. As extracellular proteins are often associated with the virulence of pathogenic bacteria, we undertook a proteomic...

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Published in:PLoS ONE
Main Authors: Madec, Stéphanie, Pichereau, Vianney, Jacq, Annick, Paillard, Mathieu, Boisset, Claire, Guérard, Fabienne, Paillard, Christine, Nicolas, Jean-Louis
Other Authors: Laboratoire Universitaire de Biodiversité et Ecologie Microbienne (LUBEM), Université de Brest (UBO), Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR), Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM), Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Institut de génétique et microbiologie Orsay (IGM), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Centre de Recherches sur les Macromolécules Végétales (CERMAV), Université Joseph Fourier - Grenoble 1 (UJF)-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS), European Project: 266157,EC:FP7:KBBE,FP7-KBBE-2010-4,BIVALIFE(2011)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2014
Subjects:
ACL
Online Access:https://hal.univ-brest.fr/hal-01096899
https://hal.univ-brest.fr/hal-01096899/document
https://hal.univ-brest.fr/hal-01096899/file/Plos-Madec-2014pdf.pdf
https://doi.org/10.1371/journal.pone.0113097
id ftunivbrest:oai:HAL:hal-01096899v1
record_format openpolar
institution Open Polar
collection Université de Bretagne Occidentale: HAL
op_collection_id ftunivbrest
language English
topic METALLOPROTEASE
ACL
BROWN RING DISEASE
OYSTER CRASSOSTREA-GIGAS
AUTOPROCESSING RTX TOXIN
RUDITAPES-PHILIPPINARUM
PROTEOMIC ANALYSIS
MANILA CLAM
VIRULENCE
TAPETIS
CHOLERAE
[SDV]Life Sciences [q-bio]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle METALLOPROTEASE
ACL
BROWN RING DISEASE
OYSTER CRASSOSTREA-GIGAS
AUTOPROCESSING RTX TOXIN
RUDITAPES-PHILIPPINARUM
PROTEOMIC ANALYSIS
MANILA CLAM
VIRULENCE
TAPETIS
CHOLERAE
[SDV]Life Sciences [q-bio]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Madec, Stéphanie
Pichereau, Vianney
Jacq, Annick
Paillard, Mathieu
Boisset, Claire
Guérard, Fabienne
Paillard, Christine
Nicolas, Jean-Louis
Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks
topic_facet METALLOPROTEASE
ACL
BROWN RING DISEASE
OYSTER CRASSOSTREA-GIGAS
AUTOPROCESSING RTX TOXIN
RUDITAPES-PHILIPPINARUM
PROTEOMIC ANALYSIS
MANILA CLAM
VIRULENCE
TAPETIS
CHOLERAE
[SDV]Life Sciences [q-bio]
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description International audience Vibrio tapetis causes the brown ring disease in the Japanese clam Ruditapes philippinarum while Vibrio aestuarianus is associated with massive oyster mortalities. As extracellular proteins are often associated with the virulence of pathogenic bacteria, we undertook a proteomic approach to characterize the secretomes of both vibrios. The extracellular proteins (ECPs) of both species were fractionated by SEC-FPLC and in vitro assays were performed to measure the effects of each fraction on hemocyte cellular parameters (phagocytosis and adhesion). Fractions showing a significant effect were subjected to SDS-PAGE, and proteins were identified by nano LC-MS/MS. 45 proteins were identified for V. aestuarianus and 87 for V. tapetis. Most of them belonged to outer membrane or were periplasmic, including porins or adhesins that were already described as virulence factors in other bacterial species. Others were transporter components, flagella proteins, or proteins of unknown function (14 and 15 respectively). Interestingly, for V. aestuarianus, we noted the secretion of 3 extracellular enzymes including the Vam metalloprotease and two other enzymes (one putative lipase and one protease). For V. tapetis, we identified five extracellular enymes, i.e. two different endochitinases, one protease, one lipase and an adhesin. A comparison of both secretomes also showed that only the putative extracellular lipase was common to both secretomes, underscoring the difference in pathogenicity mechanisms between these two species. Overall, these results characterize for the first time the secretomes of these two marine pathogenic vibrios and constitute a useful working basis to further analyze the contribution of specific proteins in the virulence mechanisms of these species. Citation: Madec S, Pichereau V, Jacq A, Paillard M, Boisset C, et al. (2014) Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks. PLoS ONE 9(11): e113097.
author2 Laboratoire Universitaire de Biodiversité et Ecologie Microbienne (LUBEM)
Université de Brest (UBO)
Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR)
Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM)
Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)
Institut de génétique et microbiologie Orsay (IGM)
Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS)
Centre de Recherches sur les Macromolécules Végétales (CERMAV)
Université Joseph Fourier - Grenoble 1 (UJF)-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS)
European Project: 266157,EC:FP7:KBBE,FP7-KBBE-2010-4,BIVALIFE(2011)
format Article in Journal/Newspaper
author Madec, Stéphanie
Pichereau, Vianney
Jacq, Annick
Paillard, Mathieu
Boisset, Claire
Guérard, Fabienne
Paillard, Christine
Nicolas, Jean-Louis
author_facet Madec, Stéphanie
Pichereau, Vianney
Jacq, Annick
Paillard, Mathieu
Boisset, Claire
Guérard, Fabienne
Paillard, Christine
Nicolas, Jean-Louis
author_sort Madec, Stéphanie
title Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks
title_short Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks
title_full Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks
title_fullStr Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks
title_full_unstemmed Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks
title_sort characterization of the secretomes of two vibrios pathogenic to mollusks
publisher HAL CCSD
publishDate 2014
url https://hal.univ-brest.fr/hal-01096899
https://hal.univ-brest.fr/hal-01096899/document
https://hal.univ-brest.fr/hal-01096899/file/Plos-Madec-2014pdf.pdf
https://doi.org/10.1371/journal.pone.0113097
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source ISSN: 1932-6203
EISSN: 1932-6203
PLoS ONE
https://hal.univ-brest.fr/hal-01096899
PLoS ONE, 2014, 9 (11), pp.0113097. ⟨10.1371/journal.pone.0113097⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0113097
info:eu-repo/grantAgreement/EC/FP7/266157/EU/Controlling infectious diseases in oysters and mussels in Europe/BIVALIFE
hal-01096899
https://hal.univ-brest.fr/hal-01096899
https://hal.univ-brest.fr/hal-01096899/document
https://hal.univ-brest.fr/hal-01096899/file/Plos-Madec-2014pdf.pdf
doi:10.1371/journal.pone.0113097
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1371/journal.pone.0113097
container_title PLoS ONE
container_volume 9
container_issue 11
container_start_page e113097
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spelling ftunivbrest:oai:HAL:hal-01096899v1 2024-05-12T08:02:47+00:00 Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks Madec, Stéphanie Pichereau, Vianney Jacq, Annick Paillard, Mathieu Boisset, Claire Guérard, Fabienne Paillard, Christine Nicolas, Jean-Louis Laboratoire Universitaire de Biodiversité et Ecologie Microbienne (LUBEM) Université de Brest (UBO) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut de génétique et microbiologie Orsay (IGM) Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS) Centre de Recherches sur les Macromolécules Végétales (CERMAV) Université Joseph Fourier - Grenoble 1 (UJF)-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS) European Project: 266157,EC:FP7:KBBE,FP7-KBBE-2010-4,BIVALIFE(2011) 2014-11 https://hal.univ-brest.fr/hal-01096899 https://hal.univ-brest.fr/hal-01096899/document https://hal.univ-brest.fr/hal-01096899/file/Plos-Madec-2014pdf.pdf https://doi.org/10.1371/journal.pone.0113097 en eng HAL CCSD Public Library of Science info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0113097 info:eu-repo/grantAgreement/EC/FP7/266157/EU/Controlling infectious diseases in oysters and mussels in Europe/BIVALIFE hal-01096899 https://hal.univ-brest.fr/hal-01096899 https://hal.univ-brest.fr/hal-01096899/document https://hal.univ-brest.fr/hal-01096899/file/Plos-Madec-2014pdf.pdf doi:10.1371/journal.pone.0113097 info:eu-repo/semantics/OpenAccess ISSN: 1932-6203 EISSN: 1932-6203 PLoS ONE https://hal.univ-brest.fr/hal-01096899 PLoS ONE, 2014, 9 (11), pp.0113097. ⟨10.1371/journal.pone.0113097⟩ METALLOPROTEASE ACL BROWN RING DISEASE OYSTER CRASSOSTREA-GIGAS AUTOPROCESSING RTX TOXIN RUDITAPES-PHILIPPINARUM PROTEOMIC ANALYSIS MANILA CLAM VIRULENCE TAPETIS CHOLERAE [SDV]Life Sciences [q-bio] [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2014 ftunivbrest https://doi.org/10.1371/journal.pone.0113097 2024-04-17T23:57:09Z International audience Vibrio tapetis causes the brown ring disease in the Japanese clam Ruditapes philippinarum while Vibrio aestuarianus is associated with massive oyster mortalities. As extracellular proteins are often associated with the virulence of pathogenic bacteria, we undertook a proteomic approach to characterize the secretomes of both vibrios. The extracellular proteins (ECPs) of both species were fractionated by SEC-FPLC and in vitro assays were performed to measure the effects of each fraction on hemocyte cellular parameters (phagocytosis and adhesion). Fractions showing a significant effect were subjected to SDS-PAGE, and proteins were identified by nano LC-MS/MS. 45 proteins were identified for V. aestuarianus and 87 for V. tapetis. Most of them belonged to outer membrane or were periplasmic, including porins or adhesins that were already described as virulence factors in other bacterial species. Others were transporter components, flagella proteins, or proteins of unknown function (14 and 15 respectively). Interestingly, for V. aestuarianus, we noted the secretion of 3 extracellular enzymes including the Vam metalloprotease and two other enzymes (one putative lipase and one protease). For V. tapetis, we identified five extracellular enymes, i.e. two different endochitinases, one protease, one lipase and an adhesin. A comparison of both secretomes also showed that only the putative extracellular lipase was common to both secretomes, underscoring the difference in pathogenicity mechanisms between these two species. Overall, these results characterize for the first time the secretomes of these two marine pathogenic vibrios and constitute a useful working basis to further analyze the contribution of specific proteins in the virulence mechanisms of these species. Citation: Madec S, Pichereau V, Jacq A, Paillard M, Boisset C, et al. (2014) Characterization of the Secretomes of Two Vibrios Pathogenic to Mollusks. PLoS ONE 9(11): e113097. Article in Journal/Newspaper Crassostrea gigas Université de Bretagne Occidentale: HAL PLoS ONE 9 11 e113097