Strain-specific quorum-sensing responses determine virulence properties in Vibrio anguillarum

Jesper Juel Mauritzen; Emilie Søndberg; Panos G. Kalatzis; Line Roager; Lone Gram; Sine Lo Svenningsen; Mathias Middelboe

doi:10.1111/1462-2920.16356

Strain-specific quorum-sensing responses determine virulence properties in Vibrio anguillarum

Jesper Juel Mauritzen^*, Emilie Søndberg, Panos G. Kalatzis, Line Roager, Lone Gram, Sine Lo Svenningsen, Mathias Middelboe^*

^*Kontaktforfatter

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

43 Downloads (Pure)

Abstract

Bacterial populations communicate using quorum-sensing (QS) molecules and switch on QS regulation to engage in coordinated behaviour such as biofilm formation or virulence. The marine fish pathogen Vibrio anguillarum harbours several QS systems, and our understanding of its QS regulation is still fragmentary. Here, we identify the VanT-QS regulon and explore the diversity and trajectory of traits under QS regulation in Vibrio anguillarum through comparative transcriptomics of two wildtype strains and their corresponding mutants artificially locked in QS-on (ΔvanO) or QS-off (ΔvanT) states. Intriguingly, the two wildtype populations showed different QS responses to cell density changes and operated primarily in the QS-on and QS-off spectrum, respectively. Examining 27 V. anguillarum strains revealed that ~11% were QS-negative, and GFP-reporter measurements of nine QS-positive strains revealed a highly strain-specific nature of the QS responses. We showed that QS controls a plethora of genes involved in processes such as central metabolism, biofilm formation, competence, T6SS, and virulence properties in V. anguillarum, with large strain-specific differences. Moreover, we demonstrated that the QS state is an important driver of virulence towards fish larvae in one of two V. anguillarum strains. We speculate that infections by mixed-strain communities spanning diverse QS strategies optimize the infection efficiency of the pathogen

Originalsprog	Engelsk
Tidsskrift	Environmental Microbiology
Vol/bind	25
Udgave nummer	7
Sider (fra-til)	1344-1362
ISSN	1462-2912
DOI	https://doi.org/10.1111/1462-2920.16356
Status	Udgivet - jul. 2023

Bibliografisk note

Funding Information:
The authors would like to thank Søs Riber & John Steffensen for providing cod blood, and Bastian Barker Rasmussen for guidance on fish cell line experiments. The authors would like to thank Bertil Gummesson for valuable discussions and suggestions on the use of spike‐in cultures. The authors thank Julia van Kessel for helpful discussions and providing plasmid pCS42. This research was funded by the University of Copenhagen, Department of Biology as a PhD stipend granted to Jesper Juel Mauritzen. Funding from the Independent Research Fund Denmark (grant 7014‐00080B), The Danish National Research Foundation (DNRF145), and the Novo Nordisk Foundation (grant NNF20OC0064249) is acknowledged. Fish larvae trials were carried out at the facilities of Hellenic Center for Marine Research with funding from AquaExcel 2020 project ( https://www.aquaexcel2020.eu/ ) with PID: AE130019.

Publisher Copyright:
© 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.

Dokumenter og links

10.1111/1462-2920.16356Licens: CC BY-NC-ND

Open Access VersionForlagets udgivne version, 2,59 MBLicens: CC BY-NC-ND

SDU link

Tjek adgangen til materialet i Syddansk Universitetsbiblioteks søgemaskine

Citationsformater

@article{76ed78b536e24a258bd6123eafef2497,

title = "Strain-specific quorum-sensing responses determine virulence properties in Vibrio anguillarum",

abstract = "Bacterial populations communicate using quorum-sensing (QS) molecules and switch on QS regulation to engage in coordinated behaviour such as biofilm formation or virulence. The marine fish pathogen Vibrio anguillarum harbours several QS systems, and our understanding of its QS regulation is still fragmentary. Here, we identify the VanT-QS regulon and explore the diversity and trajectory of traits under QS regulation in Vibrio anguillarum through comparative transcriptomics of two wildtype strains and their corresponding mutants artificially locked in QS-on (ΔvanO) or QS-off (ΔvanT) states. Intriguingly, the two wildtype populations showed different QS responses to cell density changes and operated primarily in the QS-on and QS-off spectrum, respectively. Examining 27 V. anguillarum strains revealed that ~11% were QS-negative, and GFP-reporter measurements of nine QS-positive strains revealed a highly strain-specific nature of the QS responses. We showed that QS controls a plethora of genes involved in processes such as central metabolism, biofilm formation, competence, T6SS, and virulence properties in V. anguillarum, with large strain-specific differences. Moreover, we demonstrated that the QS state is an important driver of virulence towards fish larvae in one of two V. anguillarum strains. We speculate that infections by mixed-strain communities spanning diverse QS strategies optimize the infection efficiency of the pathogen.",

keywords = "Animals, Bacterial Proteins/genetics, Gene Expression Regulation, Bacterial, Quorum Sensing/genetics, Vibrio/metabolism, Virulence/genetics",

author = "Mauritzen, {Jesper Juel} and Emilie S{\o}ndberg and Kalatzis, {Panos G.} and Line Roager and Lone Gram and Svenningsen, {Sine Lo} and Mathias Middelboe",

note = "Funding Information: The authors would like to thank S{\o}s Riber & John Steffensen for providing cod blood, and Bastian Barker Rasmussen for guidance on fish cell line experiments. The authors would like to thank Bertil Gummesson for valuable discussions and suggestions on the use of spike‐in cultures. The authors thank Julia van Kessel for helpful discussions and providing plasmid pCS42. This research was funded by the University of Copenhagen, Department of Biology as a PhD stipend granted to Jesper Juel Mauritzen. Funding from the Independent Research Fund Denmark (grant 7014‐00080B), The Danish National Research Foundation (DNRF145), and the Novo Nordisk Foundation (grant NNF20OC0064249) is acknowledged. Fish larvae trials were carried out at the facilities of Hellenic Center for Marine Research with funding from AquaExcel 2020 project ( https://www.aquaexcel2020.eu/ ) with PID: AE130019. Publisher Copyright: {\textcopyright} 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.",

year = "2023",

month = jul,

doi = "10.1111/1462-2920.16356",

language = "English",

volume = "25",

pages = "1344--1362",

journal = "Environmental Microbiology",

issn = "1462-2912",

publisher = "Wiley",

number = "7",

}

TY - JOUR

T1 - Strain-specific quorum-sensing responses determine virulence properties in Vibrio anguillarum

AU - Mauritzen, Jesper Juel

AU - Søndberg, Emilie

AU - Kalatzis, Panos G.

AU - Roager, Line

AU - Gram, Lone

AU - Svenningsen, Sine Lo

AU - Middelboe, Mathias

N1 - Funding Information: The authors would like to thank Søs Riber & John Steffensen for providing cod blood, and Bastian Barker Rasmussen for guidance on fish cell line experiments. The authors would like to thank Bertil Gummesson for valuable discussions and suggestions on the use of spike‐in cultures. The authors thank Julia van Kessel for helpful discussions and providing plasmid pCS42. This research was funded by the University of Copenhagen, Department of Biology as a PhD stipend granted to Jesper Juel Mauritzen. Funding from the Independent Research Fund Denmark (grant 7014‐00080B), The Danish National Research Foundation (DNRF145), and the Novo Nordisk Foundation (grant NNF20OC0064249) is acknowledged. Fish larvae trials were carried out at the facilities of Hellenic Center for Marine Research with funding from AquaExcel 2020 project ( https://www.aquaexcel2020.eu/ ) with PID: AE130019. Publisher Copyright: © 2023 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.

PY - 2023/7

Y1 - 2023/7

N2 - Bacterial populations communicate using quorum-sensing (QS) molecules and switch on QS regulation to engage in coordinated behaviour such as biofilm formation or virulence. The marine fish pathogen Vibrio anguillarum harbours several QS systems, and our understanding of its QS regulation is still fragmentary. Here, we identify the VanT-QS regulon and explore the diversity and trajectory of traits under QS regulation in Vibrio anguillarum through comparative transcriptomics of two wildtype strains and their corresponding mutants artificially locked in QS-on (ΔvanO) or QS-off (ΔvanT) states. Intriguingly, the two wildtype populations showed different QS responses to cell density changes and operated primarily in the QS-on and QS-off spectrum, respectively. Examining 27 V. anguillarum strains revealed that ~11% were QS-negative, and GFP-reporter measurements of nine QS-positive strains revealed a highly strain-specific nature of the QS responses. We showed that QS controls a plethora of genes involved in processes such as central metabolism, biofilm formation, competence, T6SS, and virulence properties in V. anguillarum, with large strain-specific differences. Moreover, we demonstrated that the QS state is an important driver of virulence towards fish larvae in one of two V. anguillarum strains. We speculate that infections by mixed-strain communities spanning diverse QS strategies optimize the infection efficiency of the pathogen.

AB - Bacterial populations communicate using quorum-sensing (QS) molecules and switch on QS regulation to engage in coordinated behaviour such as biofilm formation or virulence. The marine fish pathogen Vibrio anguillarum harbours several QS systems, and our understanding of its QS regulation is still fragmentary. Here, we identify the VanT-QS regulon and explore the diversity and trajectory of traits under QS regulation in Vibrio anguillarum through comparative transcriptomics of two wildtype strains and their corresponding mutants artificially locked in QS-on (ΔvanO) or QS-off (ΔvanT) states. Intriguingly, the two wildtype populations showed different QS responses to cell density changes and operated primarily in the QS-on and QS-off spectrum, respectively. Examining 27 V. anguillarum strains revealed that ~11% were QS-negative, and GFP-reporter measurements of nine QS-positive strains revealed a highly strain-specific nature of the QS responses. We showed that QS controls a plethora of genes involved in processes such as central metabolism, biofilm formation, competence, T6SS, and virulence properties in V. anguillarum, with large strain-specific differences. Moreover, we demonstrated that the QS state is an important driver of virulence towards fish larvae in one of two V. anguillarum strains. We speculate that infections by mixed-strain communities spanning diverse QS strategies optimize the infection efficiency of the pathogen.

KW - Animals

KW - Bacterial Proteins/genetics

KW - Gene Expression Regulation, Bacterial

KW - Quorum Sensing/genetics

KW - Vibrio/metabolism

KW - Virulence/genetics

U2 - 10.1111/1462-2920.16356

DO - 10.1111/1462-2920.16356

M3 - Journal article

C2 - 36807464

AN - SCOPUS:85150811536

SN - 1462-2912

VL - 25

SP - 1344

EP - 1362

JO - Environmental Microbiology

JF - Environmental Microbiology

IS - 7

ER -

Strain-specific quorum-sensing responses determine virulence properties in Vibrio anguillarum

Abstract

Bibliografisk note

Dokumenter og links

SDU link

Fingeraftryk

Citationsformater