Gonadal miRNomes and transcriptomes in infected fish reveal sexually dimorphic patterns of the immune response

IF 3.9 4区 生物学 Q1 GENETICS & HEREDITY
Tosca A. van Gelderen, Pinky Debnath, Silvia Joly, Edgar Bertomeu, Neil Duncan, Dolors Furones, Laia Ribas
{"title":"Gonadal miRNomes and transcriptomes in infected fish reveal sexually dimorphic patterns of the immune response","authors":"Tosca A. van Gelderen,&nbsp;Pinky Debnath,&nbsp;Silvia Joly,&nbsp;Edgar Bertomeu,&nbsp;Neil Duncan,&nbsp;Dolors Furones,&nbsp;Laia Ribas","doi":"10.1007/s10142-025-01537-w","DOIUrl":null,"url":null,"abstract":"<div><p>Fish disease outbreaks caused by bacterial burdens are responsible for decreasing productivity in aquaculture. Unraveling the molecular mechanisms activated in the gonads after infections is pivotal for enhancing husbandry techniques in fish farms, ensuring disease management, and selecting the most resilience phenotype. The present study, with an important commercial species the European sea bass (<i>Dicentrarchus labrax</i>), an important commercial species in Europe, examined changes in the miRNome and transcriptome 48 h after an intraperitoneal infection with <i>Vibrio anguillarum</i>. The findings indicate that following infection, testes exhibited more pronounced alterations in both the miRNome and transcriptome. Specifically, males showed approximately 26% more differentially expressed genes in testicular genes compared to females (2,624 vs. 101 DEGs). Additionally, four miRNAs (miR-183-5p, miR-191-3p, miR-451-5p, and miR-724-5p) were significantly expressed post-infection in males, while none were identified in females. Interestingly, upon deep analysis of sexual dimorphic gene modules, a larger number of miRNAs were identified in infected females targeting genes related to the immune system compared to infected males. These results suggest that fish ovaries demonstrate greater resilience in response to infections by suppressing genes related to the immune system through a post-transcriptional mechanism performed by miRNAs. In contrast, testes activate genes related to the immune system and repress genes related to cellular processes to cope with the infection. In particular, the crosstalk between the miRNome and transcriptome in infected males revealed a pivotal gene, namely, insulin-like growth factor binding protein (<i>igfbp</i>), acting as a gene network hub in which miR-192-3p was connected. The current study elucidated the need to comprehend the basic immune regulatory responses associated with miRNAs and gene regulation networks that depend on fish sex. The data reveal the importance of considering sex as a factor in interpreting the immune system in fish to generate efficient protocols to prevent outbreaks in fish farms.</p></div>","PeriodicalId":574,"journal":{"name":"Functional & Integrative Genomics","volume":"25 1","pages":""},"PeriodicalIF":3.9000,"publicationDate":"2025-01-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11782434/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Functional & Integrative Genomics","FirstCategoryId":"99","ListUrlMain":"https://link.springer.com/article/10.1007/s10142-025-01537-w","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"GENETICS & HEREDITY","Score":null,"Total":0}
引用次数: 0

Abstract

Fish disease outbreaks caused by bacterial burdens are responsible for decreasing productivity in aquaculture. Unraveling the molecular mechanisms activated in the gonads after infections is pivotal for enhancing husbandry techniques in fish farms, ensuring disease management, and selecting the most resilience phenotype. The present study, with an important commercial species the European sea bass (Dicentrarchus labrax), an important commercial species in Europe, examined changes in the miRNome and transcriptome 48 h after an intraperitoneal infection with Vibrio anguillarum. The findings indicate that following infection, testes exhibited more pronounced alterations in both the miRNome and transcriptome. Specifically, males showed approximately 26% more differentially expressed genes in testicular genes compared to females (2,624 vs. 101 DEGs). Additionally, four miRNAs (miR-183-5p, miR-191-3p, miR-451-5p, and miR-724-5p) were significantly expressed post-infection in males, while none were identified in females. Interestingly, upon deep analysis of sexual dimorphic gene modules, a larger number of miRNAs were identified in infected females targeting genes related to the immune system compared to infected males. These results suggest that fish ovaries demonstrate greater resilience in response to infections by suppressing genes related to the immune system through a post-transcriptional mechanism performed by miRNAs. In contrast, testes activate genes related to the immune system and repress genes related to cellular processes to cope with the infection. In particular, the crosstalk between the miRNome and transcriptome in infected males revealed a pivotal gene, namely, insulin-like growth factor binding protein (igfbp), acting as a gene network hub in which miR-192-3p was connected. The current study elucidated the need to comprehend the basic immune regulatory responses associated with miRNAs and gene regulation networks that depend on fish sex. The data reveal the importance of considering sex as a factor in interpreting the immune system in fish to generate efficient protocols to prevent outbreaks in fish farms.

受感染鱼类的性腺miRNomes和转录组揭示了免疫反应的两性二态模式。
由细菌负担引起的鱼类疾病暴发是导致水产养殖生产力下降的原因。揭示感染后性腺激活的分子机制对于提高养鱼场的养殖技术、确保疾病管理和选择最具弹性的表型至关重要。本研究以欧洲重要的商业物种欧洲海鲈鱼(Dicentrarchus labrax)为研究对象,研究了腹腔感染鳗弧菌48小时后miRNome和转录组的变化。研究结果表明,感染后,睾丸在miRNome和转录组中都表现出更明显的改变。具体来说,男性在睾丸基因中的差异表达基因比女性多26%(2624对101)。此外,四种mirna (miR-183-5p、miR-191-3p、miR-451-5p和miR-724-5p)在男性感染后显著表达,而在女性中没有发现。有趣的是,通过对两性二态基因模块的深入分析,与感染的男性相比,在感染的女性中发现了更多的靶向免疫系统相关基因的mirna。这些结果表明,鱼类卵巢通过mirna的转录后机制抑制与免疫系统相关的基因,从而表现出更强的抗感染能力。相反,睾丸激活与免疫系统相关的基因,抑制与细胞过程相关的基因来应对感染。特别是,受感染男性miRNome和转录组之间的串扰揭示了一个关键基因,即胰岛素样生长因子结合蛋白(igfbp),它作为连接miR-192-3p的基因网络枢纽。目前的研究阐明了了解与mirna和依赖于鱼类性别的基因调控网络相关的基本免疫调节反应的必要性。这些数据揭示了将性别作为解释鱼类免疫系统的一个因素来制定有效的方案以防止养鱼场爆发的重要性。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
CiteScore
3.50
自引率
3.40%
发文量
92
审稿时长
2 months
期刊介绍: Functional & Integrative Genomics is devoted to large-scale studies of genomes and their functions, including systems analyses of biological processes. The journal will provide the research community an integrated platform where researchers can share, review and discuss their findings on important biological questions that will ultimately enable us to answer the fundamental question: How do genomes work?
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信