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Cyclic di-GMP inactivates T6SS and T4SS activity in agrobacterium tumefaciens

Cyclic di-GMP inactivates T6SS and T4SS activity in agrobacterium tumefaciens
Cyclic di-GMP inactivates T6SS and T4SS activity in agrobacterium tumefaciens

The Type VI secretion system (T6SS) is a bacterial nanomachine that delivers effector proteins into prokaryotic and eukaryotic preys. This secretion system has emerged as a key player in regulating the microbial diversity in a population. In the plant pathogen Agrobacterium tumefaciens, the signalling cascades regulating the activity of this secretion system are poorly understood. Here, we outline how the universal eubacterial second messenger cyclic di-GMP impacts the production of T6SS toxins and T6SS structural components. We demonstrate that this has a significant impact on the ability of the phytopathogen to compete with other bacterial species in vitro and in planta. Our results suggest that, as opposed to other bacteria, c-di-GMP turns down the T6SS in A. tumefaciens thus impacting its ability to compete with other bacterial species within the rhizosphere. We also demonstrate that elevated levels of c-di-GMP within the cell decrease the activity of the Type IV secretion system (T4SS) and subsequently the capacity of A. tumefaciens to transform plant cells. We propose that such peculiar control reflects on c-di-GMP being a key second messenger that silences energy-costing systems during early colonization phase and biofilm formation, while low c-di-GMP levels unleash T6SS and T4SS to advance plant colonization.

Agrobacterium tumefaciens/genetics, Bacterial Proteins/genetics, Cyclic GMP/analogs & derivatives, Gene Expression Regulation, Bacterial, Type IV Secretion Systems/genetics, Type VI Secretion Systems/genetics
0950-382X
632-648
McCarthy, Ronan R
0b2cf2e0-b0ff-4c92-aa04-92d91182d1f2
Yu, Manda
85c96472-f5ea-4710-8b9a-e492b9c9e1b4
Eilers, Kira
15f54fcf-e200-4511-9dbf-71d50c993ba5
Wang, Yi-Chieh
8e501f8b-93a5-4e87-b781-da84a79cb18e
Lai, Erh-Min
730dfb33-66f8-48d6-8c0c-9a42cc5a095b
Filloux, Alain
6f79a42e-17d2-4fb1-bab9-a27c41a5b029
McCarthy, Ronan R
0b2cf2e0-b0ff-4c92-aa04-92d91182d1f2
Yu, Manda
85c96472-f5ea-4710-8b9a-e492b9c9e1b4
Eilers, Kira
15f54fcf-e200-4511-9dbf-71d50c993ba5
Wang, Yi-Chieh
8e501f8b-93a5-4e87-b781-da84a79cb18e
Lai, Erh-Min
730dfb33-66f8-48d6-8c0c-9a42cc5a095b
Filloux, Alain
6f79a42e-17d2-4fb1-bab9-a27c41a5b029

McCarthy, Ronan R, Yu, Manda, Eilers, Kira, Wang, Yi-Chieh, Lai, Erh-Min and Filloux, Alain (2019) Cyclic di-GMP inactivates T6SS and T4SS activity in agrobacterium tumefaciens. Molecular Microbiology, 112 (2), 632-648. (doi:10.1111/mmi.14279).

Record type: Article

Abstract

The Type VI secretion system (T6SS) is a bacterial nanomachine that delivers effector proteins into prokaryotic and eukaryotic preys. This secretion system has emerged as a key player in regulating the microbial diversity in a population. In the plant pathogen Agrobacterium tumefaciens, the signalling cascades regulating the activity of this secretion system are poorly understood. Here, we outline how the universal eubacterial second messenger cyclic di-GMP impacts the production of T6SS toxins and T6SS structural components. We demonstrate that this has a significant impact on the ability of the phytopathogen to compete with other bacterial species in vitro and in planta. Our results suggest that, as opposed to other bacteria, c-di-GMP turns down the T6SS in A. tumefaciens thus impacting its ability to compete with other bacterial species within the rhizosphere. We also demonstrate that elevated levels of c-di-GMP within the cell decrease the activity of the Type IV secretion system (T4SS) and subsequently the capacity of A. tumefaciens to transform plant cells. We propose that such peculiar control reflects on c-di-GMP being a key second messenger that silences energy-costing systems during early colonization phase and biofilm formation, while low c-di-GMP levels unleash T6SS and T4SS to advance plant colonization.

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More information

Published date: August 2019
Additional Information: © 2019 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
Keywords: Agrobacterium tumefaciens/genetics, Bacterial Proteins/genetics, Cyclic GMP/analogs & derivatives, Gene Expression Regulation, Bacterial, Type IV Secretion Systems/genetics, Type VI Secretion Systems/genetics

Identifiers

Local EPrints ID: 506096
URI: http://eprints.soton.ac.uk/id/eprint/506096
ISSN: 0950-382X
PURE UUID: 0d622c3c-c0e6-4d98-b231-439acd36e53e
ORCID for Ronan R McCarthy: ORCID iD orcid.org/0000-0002-7480-6352

Catalogue record

Date deposited: 28 Oct 2025 18:25
Last modified: 29 Oct 2025 03:15

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Contributors

Author: Ronan R McCarthy ORCID iD
Author: Manda Yu
Author: Kira Eilers
Author: Yi-Chieh Wang
Author: Erh-Min Lai
Author: Alain Filloux

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