Type IV secretion system effector sabotages multiple defense systems in a competing bacterium.

T4SS LuxR Lysobacter Pseudomonas PvdS antimicrobial activity effector

Journal

The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086

Informations de publication

Date de publication:
03 Jul 2024
Historique:
received: 25 03 2024
revised: 22 06 2024
accepted: 02 07 2024
medline: 4 7 2024
pubmed: 4 7 2024
entrez: 3 7 2024
Statut: aheadofprint

Résumé

Effector proteins secreted by bacteria that infect mammalian and plant cells often subdue eukaryotic host cell defenses by simultaneously affecting multiple targets. However, instances when a bacterial effector injected in the competing bacteria sabotage more than a single target have not been reported. Here, we demonstrate that the effector protein, LtaE, translocated by the type IV secretion system (T4SS) from the soil bacterium Lysobacter enzymogenes into the competing bacterium, Pseudomonas protegens, affects several targets, thus disabling the antibacterial defenses of the competitor. One LtaE target is the transcription factor, LuxR1, that regulates biosynthesis of the antimicrobial compound, orfamide A. Another target is the sigma factor, PvdS, required for biosynthesis of another antimicrobial compound, pyoverdine. Deletion of the genes involved in orfamide A and pyoverdine biosynthesis disabled the antibacterial activity of P. protegens, whereas expression of LtaE in P. protegens resulted in the near-complete loss of the antibacterial activity against L. enzymogenes. Mechanistically, LtaE inhibits the assembly of the RNA polymerase complexes with each of these proteins. The ability of LtaE to bind to LuxR1 and PvdS homologs from several Pseudomonas species suggests that it can sabotage defenses of various competitors present in the soil or on plant matter. Our study thus reveals that the multi-target effectors have evolved to subdue cell defenses not only in eukaryotic hosts but also in bacterial competitors.

Identifiants

pubmed: 38959853
pii: 7705541
doi: 10.1093/ismejo/wrae121
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) [2024]. Published by Oxford University Press on behalf of the International Society for Microbial Ecology.

Auteurs

Bingxin Wang (B)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Fugui Xu (F)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Zeyu Zhang (Z)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Danyu Shen (D)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Limin Wang (L)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Huijun Wu (H)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Qing Yan (Q)

Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, Montana 59717, United States.

Chuanbin Cui (C)

Shaanxi Provincial Tobacco Corporation of CNTC, Xi'an 710061, China.

Pingping Wang (P)

Shaanxi Provincial Tobacco Corporation of CNTC, Xi'an 710061, China.

Qi Wei (Q)

Industrial Crops Institute, Heilongjiang Academy of Agricultural Sciences, Harbin 150086, China.

Xiaolong Shao (X)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Mengcen Wang (M)

State Key Laboratory of Rice Biology and Breeding, Zhejiang University, Hangzhou 310058, China.
Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Pesticide and Environmental Toxicology, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China.

Guoliang Qian (G)

College of Plant Protection (Key Laboratory of Integrated Management of Crop Diseases and Pests), Nanjing Agricultural University, Nanjing 210095, P.R. China.

Classifications MeSH