Exploitation of multiple host-derived nutrients by the yellow catfish epidermal environment facilitates Vibrio mimicus to sustain infection potency and susceptibility

• Published in: Fish & shellfish immunology Vol. 151; p. 109707
• Main Authors: Feng, Yang, Wang, Jiao, Fan, Wei, Huang, Bowen, Qin, Zhenyang, Tian, Ziqi, Geng, Yi, Huang, Xiaoli, Ouyang, Ping, Chen, Defang, Lai, Weimin
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01.08.2024
• Subjects: Host-microbe interactions; Metabolomics; Susceptibility; Vibrio mimicus; Yellow catfish (Pelteobagrus fulvidraco); Host-microbe interactions; Metabolomics; Vibrio mimicus; Susceptibility; Yellow catfish (Pelteobagrus fulvidraco)
• ISSN: 1050-4648; 1095-9947; 1095-9947
• DOI: 10.1016/j.fsi.2024.109707

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. •The research offered fresh insights into the pathogenesis of Vibrio mimicus in the yellow catfish host.•V. mimicus completes infection by enhancing metabolism, utilizing oligopeptides and nucleotides.•Yellow catfish body surface, rich in nucleotides, amino acids, and peptides, affects V. mimicus growth and motility.•Yellow catfish displayed deficiency in polyunsaturated fatty acids, impacting anti-inflammatory mechanisms.