Exploitation of Multiple Host-Derived Nutrients by the Yellow Catfish Epidermal Environment Facilitates Vibrio mimicus to Sustain Infection Potency and Susceptibility.

Host-microbe interactions Metabolomics Susceptibility Vibrio mimicus Yellow catfish (Pelteobagrus fulvidraco)

Journal

Fish & shellfish immunology
ISSN: 1095-9947
Titre abrégé: Fish Shellfish Immunol
Pays: England
ID NLM: 9505220

Informations de publication

Date de publication:
15 Jun 2024
Historique:
received: 25 02 2024
revised: 12 06 2024
accepted: 14 06 2024
medline: 18 6 2024
pubmed: 18 6 2024
entrez: 17 6 2024
Statut: aheadofprint

Résumé

Infection with Vibrio mimicus in the Siluriformes has demonstrated a rapid and high infectivity and mortality rate, distinct from other hosts. Our earlier investigations identified necrosis, an inflammatory storm, and tissue remodeling as crucial pathological responses in yellow catfish (Pelteobagrus fulvidraco) infected with V. mimicus. The objective of this study was to further elucidate the impact linking these pathological responses within the host during V. mimicus infection. Employing metabolomics and transcriptomics, we uncovered infection-induced dense vacuolization of perimysium; Several genes related to nucleosidase and peptidase activities were significantly upregulated in the skin and muscles of infected fish. Concurrently, the translation processes of host cells were impaired. Further investigation revealed that V. mimicus completes its infection process by enhancing its metabolism, including the utilization of oligopeptides and nucleotides. The high susceptibility of yellow catfish to V. mimicus infection was associated with the composition of its body surface, which provided a microenvironment rich in various nucleotides such as dIMP, dAMP, deoxyguanosine, and ADP, in addition to several amino acids and peptides. Some of these metabolites significantly boost V. mimicus growth and motility, thus influencing its biological functions. Furthermore, we uncovered an elevated expression of gangliosides on the surface of yellow catfish, aiding V. mimicus adhesion and increasing its infection risk. Notably, we observed that the skin and muscles of yellow catfish were deficient in over 25 polyunsaturated fatty acids, such as Eicosapentaenoic acid, 12-oxo-ETE, and 13-Oxo-ODE. These substances play a role in anti-inflammatory mechanisms, possibly contributing to the immune dysregulation observed in yellow catfish. In summary, our study reveals a host immune deviation phenomenon that promotes bacterial colonization by increasing nutrient supply. It underscores the crucial factors rendering yellow catfish highly susceptible to V. mimicus, indicating that host nutritional sources not only enable the establishment and maintenance of infection within the host but also aid bacterial survival under immune pressure, ultimately completing its lifecycle.

Identifiants

pubmed: 38885802
pii: S1050-4648(24)00352-8
doi: 10.1016/j.fsi.2024.109707
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

109707

Informations de copyright

Copyright © 2024. Published by Elsevier Ltd.

Déclaration de conflit d'intérêts

Declaration of Competing Interest All authors read and approved the final manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Auteurs

Yang Feng (Y)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China; Fisheries Institute, Sichuan Academy of Agricultural Sciences, Chengdu 611731, Sichuan, China.

Jiao Wang (J)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Wei Fan (W)

NeiJiang Academy of Agricultural Sciences, Neijiang, Sichuan 641000, China.

Bowen Huang (B)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Zhenyang Qin (Z)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Ziqi Tian (Z)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Yi Geng (Y)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China. Electronic address: gengyisicau@126.com.

Xiaoli Huang (X)

Department of Aquaculture, College of Animal Science & Technology, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Ping Ouyang (P)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Defang Chen (D)

Department of Aquaculture, College of Animal Science & Technology, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Weimin Lai (W)

College of Veterinary Medicine, Sichuan Agricultural University, Wenjiang 611130, Sichuan, China.

Classifications MeSH