Effect of Ichthyophthirius multifiliis infection on host immunity and microbiota shifts of Takifugu fasciatus

Xiang Gong; Yue Zhu; Xianhui Ning; Kai Zhang; Tao Wang; Shaowu Yin; Jie Ji

doi:10.1016/j.micpath.2025.107784

Effect of Ichthyophthirius multifiliis infection on host immunity and microbiota shifts of Takifugu fasciatus

Microb Pathog. 2025 Jun 3:206:107784. doi: 10.1016/j.micpath.2025.107784. Online ahead of print.

Authors

Xiang Gong¹, Yue Zhu¹, Xianhui Ning², Kai Zhang², Tao Wang², Shaowu Yin³, Jie Ji⁴

Affiliations

¹ College of Marine Science and Engineering, Nanjing Normal University, Jiangsu Province Engineering Research Center for Aquatic Animals Breeding and Green Efficient Aquacultural Technology, Jiangsu Key Laboratory of Ocean-Land Environmental Change and Ecological Construction, Nanjing, 210023, Jiangsu, China.
² College of Marine Science and Engineering, Nanjing Normal University, Jiangsu Province Engineering Research Center for Aquatic Animals Breeding and Green Efficient Aquacultural Technology, Jiangsu Key Laboratory of Ocean-Land Environmental Change and Ecological Construction, Nanjing, 210023, Jiangsu, China; Co-Innovation Center for Marine Bio-Industry Technology of Jiangsu Province, Lianyungang, 222005, China.
³ College of Marine Science and Engineering, Nanjing Normal University, Jiangsu Province Engineering Research Center for Aquatic Animals Breeding and Green Efficient Aquacultural Technology, Jiangsu Key Laboratory of Ocean-Land Environmental Change and Ecological Construction, Nanjing, 210023, Jiangsu, China; Co-Innovation Center for Marine Bio-Industry Technology of Jiangsu Province, Lianyungang, 222005, China. Electronic address: yinshaowu@163.com.
⁴ College of Marine Science and Engineering, Nanjing Normal University, Jiangsu Province Engineering Research Center for Aquatic Animals Breeding and Green Efficient Aquacultural Technology, Jiangsu Key Laboratory of Ocean-Land Environmental Change and Ecological Construction, Nanjing, 210023, Jiangsu, China; Co-Innovation Center for Marine Bio-Industry Technology of Jiangsu Province, Lianyungang, 222005, China. Electronic address: jie.ji@njnu.edu.cn.

PMID: 40473131
DOI: 10.1016/j.micpath.2025.107784

Abstract

Ichthyophthirius multifiliis (Ich) is a major pathogen responsible for high mortality rates in Takifugu fasciatus aquaculture. Despite its significance, the local and systemic immune responses of pufferfish to Ich infection remain poorly understood. Additionally, the interaction between ectoparasite infection and gut microbiota has not been thoroughly investigated. To address these gaps, we established an Ich infection model in pufferfish through bath administration. RT-PCR confirmed that Ich invades the skin, gill, and fin at 10 days post-infection (dpi) using 5000 theronts per fish. RT-qPCR analysis revealed immune responses in the spleen, liver, gill, skin, and gut following infection, while H&E staining identified Ich intrusion into the epidermal layer of the skin. RNA-seq analysis showed that pathways such as Th1 and Th2 cell differentiation, legionellosis, and Chagas disease were significantly enriched in the spleen, whereas ECM-receptor interaction, calcium signaling, and PI3K-Akt signaling pathways were enriched in the skin, suggesting that Ich breaches local defenses and activates systemic immune responses. Furthermore, Ich infection reduced the alpha diversity of the gut microbiota, with notable compositional shifts, including a decrease in commensals such as Chryseobacterium and an increase in opportunistic bacteria like Elizabethkingia. These findings enhance our understanding of the intricate interactions between parasite, host, and gut microbiota, providing insights into the immune and microbiome dynamics of Ich infection in pufferfish.

Keywords: Gut microbiome; Ichthyophthirius multifiliis; Takifugu fasciatus; Transcriptome.