Transcriptome analyses of mRNA and circular RNA reveal dietary supplementation with freeze-dried Lactiplantibacillus plantarum primes immune memory of Whiteleg shrimp (Penaeus vannamei) against pathogens

IF 4.1 2区农林科学 Q1 FISHERIES

Fish & shellfish immunology Pub Date : 2025-02-01 DOI:10.1016/j.fsi.2024.110091

John Paul Matthew Domingo Guzman , Reiko Nozaki , Mikio Aoki , Hiroshi Kuwahara , Kazuki Mikata , Keiichiro Koiwai , Hidehiro Kondo , Ikuo Hirono

{"title":"Transcriptome analyses of mRNA and circular RNA reveal dietary supplementation with freeze-dried Lactiplantibacillus plantarum primes immune memory of Whiteleg shrimp (Penaeus vannamei) against pathogens","authors":"John Paul Matthew Domingo Guzman , Reiko Nozaki , Mikio Aoki , Hiroshi Kuwahara , Kazuki Mikata , Keiichiro Koiwai , Hidehiro Kondo , Ikuo Hirono","doi":"10.1016/j.fsi.2024.110091","DOIUrl":null,"url":null,"abstract":"<div><div>The lack of a classical adaptive immunity renders the development of disease control and prevention measures in shrimp challenging. In this study, the concept of trained immunity was exploited in the development of a feed supplement. <em>Penaeus vannamei</em> shrimp was fed with feed supplemented with freeze-dried whole culture of <em>Lactiplantibacillus plantarum</em> (FD-LAB) for 15 days. RNA sequencing using Illumina platform was performed on the gill and stomach tissues collected at specific time points during the feeding period (0<sup>th</sup> day, 8th day, 15th day). Differentially-expressed genes (DEGs) previously reported to have innate immunity- and immune memory-related functions were selected for validation. Additionally, the differential expression of putatively immune-related circular RNAs (DECs) were also explored as these noncoding regulatory RNAs may also influence host immunity. Challenge tests with either the acute hepatopancreatic necrosis disease-causing strain <em>Vibrio parahaemolyticus</em> D6 or White Spot Syndrome Virus (WSSV) were conducted. Transcriptome analyses showed that FD-LAB supplementation resulted to DEGs and DECs related to pathogen recognition, antimicrobial peptides, transcription regulation, and immune memory. Challenge tests performed immediately after 15 days and 8 days of feeding showed protection on <em>P. vannamei</em> by FD-LAB against bacterial and viral pathogens. Increase in survival rates were also observed upon challenge with both pathogens 7 days and 14 days after last intake of FD-LAB, indicating trained immunity in shrimp. Our study highlighted the effects of FD-LAB on the innate immunity and immune memory of <em>P. vannamei</em> against bacterial and viral pathogens. These findings emphasize the possibility of immunostimulants inducing lasting enhanced immunity against infections despite the lack of a classical adaptive immunity in shrimp.</div></div>","PeriodicalId":12127,"journal":{"name":"Fish & shellfish immunology","volume":"157 ","pages":"Article 110091"},"PeriodicalIF":4.1000,"publicationDate":"2025-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Fish & shellfish immunology","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S105046482400737X","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"FISHERIES","Score":null,"Total":0}

引用次数: 0

Abstract

The lack of a classical adaptive immunity renders the development of disease control and prevention measures in shrimp challenging. In this study, the concept of trained immunity was exploited in the development of a feed supplement. Penaeus vannamei shrimp was fed with feed supplemented with freeze-dried whole culture of Lactiplantibacillus plantarum (FD-LAB) for 15 days. RNA sequencing using Illumina platform was performed on the gill and stomach tissues collected at specific time points during the feeding period (0^th day, 8th day, 15th day). Differentially-expressed genes (DEGs) previously reported to have innate immunity- and immune memory-related functions were selected for validation. Additionally, the differential expression of putatively immune-related circular RNAs (DECs) were also explored as these noncoding regulatory RNAs may also influence host immunity. Challenge tests with either the acute hepatopancreatic necrosis disease-causing strain Vibrio parahaemolyticus D6 or White Spot Syndrome Virus (WSSV) were conducted. Transcriptome analyses showed that FD-LAB supplementation resulted to DEGs and DECs related to pathogen recognition, antimicrobial peptides, transcription regulation, and immune memory. Challenge tests performed immediately after 15 days and 8 days of feeding showed protection on P. vannamei by FD-LAB against bacterial and viral pathogens. Increase in survival rates were also observed upon challenge with both pathogens 7 days and 14 days after last intake of FD-LAB, indicating trained immunity in shrimp. Our study highlighted the effects of FD-LAB on the innate immunity and immune memory of P. vannamei against bacterial and viral pathogens. These findings emphasize the possibility of immunostimulants inducing lasting enhanced immunity against infections despite the lack of a classical adaptive immunity in shrimp.

查看原文本刊更多论文

mRNA 和环状 RNA 的转录组分析表明，通过膳食补充冻干植物乳杆菌可增强白对虾（Penaeus vannamei）对病原体的免疫记忆。

缺乏经典的适应性免疫使得对虾疾病控制和预防措施的发展具有挑战性。在本研究中，训练免疫的概念被用于饲料添加剂的开发。在饲料中添加植物乳杆菌（FD-LAB）冻干全培养物，饲喂凡纳滨对虾15 d。利用Illumina平台对采食期（第0天、第8天、第15天）特定时间点采集的鳃和胃组织进行RNA测序。之前报道的具有先天免疫和免疫记忆相关功能的差异表达基因（DEGs）被选中进行验证。此外，研究人员还探讨了推定免疫相关环状rna （DECs）的差异表达，因为这些非编码调节rna也可能影响宿主免疫。用急性肝胰腺坏死致病菌株副溶血性弧菌D6或白斑综合征病毒（WSSV）进行攻毒试验。转录组分析显示，补充FD-LAB可产生与病原体识别、抗菌肽、转录调节和免疫记忆相关的deg和DECs。饲养15天和饲养8天后立即进行的攻毒试验显示，FD-LAB对凡纳美弓形虫具有抵抗细菌和病毒病原体的保护作用。在最后一次摄入FD-LAB后的第7天和第14天，两种病原体的攻击也观察到存活率的增加，这表明对虾的免疫力得到了训练。本研究重点研究了FD-LAB对凡纳梅对细菌和病毒病原体的先天免疫和免疫记忆的影响。这些发现强调了免疫刺激剂诱导持久增强抗感染免疫的可能性，尽管虾缺乏经典的适应性免疫。

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

Fish & shellfish immunology 农林科学-海洋与淡水生物学

CiteScore

7.50

自引率

19.10%

发文量

750

审稿时长

68 days

期刊介绍： Fish and Shellfish Immunology rapidly publishes high-quality, peer-refereed contributions in the expanding fields of fish and shellfish immunology. It presents studies on the basic mechanisms of both the specific and non-specific defense systems, the cells, tissues, and humoral factors involved, their dependence on environmental and intrinsic factors, response to pathogens, response to vaccination, and applied studies on the development of specific vaccines for use in the aquaculture industry.