LygA retention on the surface of Listeria monocytogenes via its interaction with wall teichoic acid modulates bacterial homeostasis and virulence.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
06 2023
Historique:
received: 18 10 2022
accepted: 13 06 2023
revised: 11 07 2023
medline: 13 7 2023
pubmed: 28 6 2023
entrez: 28 6 2023
Statut: epublish

Résumé

Wall teichoic acid (WTA) is the abundant cell wall-associated glycopolymer in Gram-positive bacteria, playing crucial roles in surface proteins retention, bacterial homeostasis, and virulence. The WTA glycosylation of Listeria monocytogenes is essential for surface anchoring of virulence factors, whereas the nature and function of the noncovalent interactions between cell wall-associated proteins and WTA are less unknown. In this study, we found that galactosylated WTA (Gal-WTA) of serovar (SV) 4h L. monocytogenes plays a key role in modulating the novel glycine-tryptophan (GW) domain-containing autolysin protein LygA through direct interactions. Gal-deficient WTA of Lm XYSN (ΔgalT) showed a dramatic reduction of LygA on the cell surface. We demonstrated that LygA binds to Gal-WTA through the GW domains, and the binding affinity is associated with the number of GW motifs. Moreover, we confirmed the direct Gal-dependent binding of the GW protein Auto from the type I WTA strain, which has no interaction with rhamnosylated WTA, indicating that the complexity of both WTA and GW proteins affect the coordination patterns. Importantly, we revealed the crucial roles of LygA in facilitating bacterial homeostasis as well as crossing the intestinal and blood-brain barriers. Altogether, our findings suggest that both the glycosylation patterns of WTA and a fixed numbers of GW domains are closely associated with the retention of LygA on the cell surface, which promotes the pathogenesis of L. monocytogenes within the host.

Identifiants

pubmed: 37379353
doi: 10.1371/journal.ppat.1011482
pii: PPATHOGENS-D-22-01788
pmc: PMC10335673
doi:

Substances chimiques

Virulence Factors 0
Membrane Proteins 0
Teichoic Acids 0
Bacterial Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1011482

Informations de copyright

Copyright: © 2023 Yao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Hao Yao (H)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Guo Li (G)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Xianglian Xiong (X)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Fanxin Jin (F)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Sirui Li (S)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Xinyu Xie (X)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Dan Zhong (D)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Renling Zhang (R)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Fanzeng Meng (F)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Yuelan Yin (Y)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

Xin'an Jiao (X)

Jiangsu Key Laboratory of Zoonosis, Yangzhou University, Yangzhou, China.
Key Laboratory of Prevention and Control of Biological Hazard Factors (Animal Origin) for Agrifood Safety and Quality, MOA of China, Yangzhou, Jiangsu Province, China.
Joint International Research Laboratory of Agriculture and Agri-product Safety of the Ministry of Education, Yangzhou, Jiangsu Province, China.
Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Disease and Zoonoses, Yangzhou, Jiangsu Province, China.

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