Cyprinid herpesvirus 2 infection changes microbiota and metabolites in the gibel carp (Carassius auratus gibelio) midgut

Front Cell Infect Microbiol. 2023 Feb 2:12:1017165. doi: 10.3389/fcimb.2022.1017165. eCollection 2022.

Abstract

Cyprinid herpesvirus 2 (CyHV-2) infects gibel carp (Carassius auratus gibelio) and causes severe losses. Microbiota in animal guts involves nutrition intake, development, immunity, and disease resistance. However, the relationship between gibel carp gut microbiota and CyHV-2 infection is not well known. Herein, we analyzed the gut microbiota composition and metabolite profiles in CyHV-2-infected and -uninfected fish using high-throughput sequencing and gas chromatography/mass spectrometry. Results showed that CyHV-2 infection significantly changed gut microbiota and metabolite profiles (p < 0.05). High-throughput sequencing demonstrated that the relative abundance of Aeromonas in the midgut increased dramatically while Cetobacterium decreased. Time-course analysis showed that the number of Aeromonas in the midgut of infected fish increased more than 1,000 times within 5 days post infection. Metabolome analysis illustrated that CyHV-2 infection significantly altered 24 metabolites in the midgut of gibel carp, annotating to the anomaly of digestion and metabolisms of amino acids, carbohydrates, and lipids, such as tryptophan (Trp) metabolism. The Mantel test demonstrated that gut microbiota and metabolite profiles were well related (r = 0.89). Furthermore, Trp metabolism responded to CyHV-2 infection closely was taken as one example to prove the correlation among CyHV-2 infection, metabolites and microbiota in the midgut, and host immunity. Results showed that modulating Trp metabolism could affect the relative abundance of Aeromonas in the midgut of fish, transcription of antiviral cytokines, and CyHV-2 infection. Therefore, we can conclude that CyHV-2 infection significantly perturbed the gut microbiome, disrupted its' metabolic functions, and caused the proliferation of the opportunistic pathogen Aeromonas. This study also suggests that modulation of the gut microbiome will open a therapeutic opportunity to control CyHV-2 infection in gibel carp.

Keywords: Aeromonas; Cetobacterium; CyHV-2; gut microbiota-mediated metabolites; tryptophan metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Fish Diseases* / microbiology
  • Gastrointestinal Microbiome*
  • Goldfish
  • Herpesviridae Infections*
  • Herpesviridae*

Supplementary concepts

  • Cyprinid herpesvirus 2

Grants and funding

This research was financially supported by the Projects on High-Quality Development of Fisheries of Yancheng (YCSCY2021020) and by the National Nature Science Foundation of China (Grant no. 32071615), and partially by the Nature Science Foundation of Jiangsu Province (BK20191044) and Basic Scientific Research Fund Project of the China Academy of Fishery Sciences (2020TD56), National Key R&D Program of China (2019YFD0900302, 2020YFD0900701), and Modern Agricultural Industry Technology System (JATS[2022]254).