Shrimp shapes a resistance trait against vibriosis by memorizing the colonization resistance of intestinal microbiota

doi:10.1371/journal.ppat.1012321

IOCAS-IR > 实验海洋生物学重点实验室

	Shrimp shapes a resistance trait against vibriosis by memorizing the colonization resistance of intestinal microbiota
	Yuan, Jianbo 1,2; Yu, Yang1,2 ; Li, Shihao 1,2; Zhang, Xiaojun 1,2; Zhang, Chuntao 1,3; Li, Roujing 1; Hu, Jie 1; Si, Shuqing 1,3; Zhang, Chengyi 1,3; Xiang, Jianhai1,2 ; Li, Fuhua 1,2
	2024-07-01
发表期刊	PLOS PATHOGENS
ISSN	1553-7366
卷号	20 期号:7 页码:26
通讯作者	Li, Fuhua(fhli@qdio.ac.cn)
摘要	Vibriosis is one of the most serious diseases that commonly occurs in aquatic animals, thus, shaping a steady inherited resistance trait in organisms has received the highest priority in aquaculture. Whereas, the mechanisms underlying the development of such a resistance trait are mostly elusive. In this study, we constructed vibriosis-resistant and susceptible families of the Pacific white shrimp Litopenaeus vannamei after four generations of artificial selection. Microbiome sequencing indicated that shrimp can successfully develop a colonization resistance trait against Vibrio infections. This trait was characterized by a microbial community structure with specific enrichment of a single probiotic species (namely Shewanella algae), and notably, its formation was inheritable and might be memorized by host epigenetic remodeling. Regardless of the infection status, a group of genes was specifically activated in the resistant family through disruption of complete methylation. Specifically, hypo-methylation and hyper-expression of genes related to lactate dehydrogenase (LDH) and iron homeostasis might provide rich sources of specific carbon (lactate) and ions for the colonization of S. algae, which directly results in the reduction of Vibrio load in shrimp. Lactate feeding increased the survival of shrimp, while knockdown of LDH gene decreased the survival when shrimp was infected by Vibrio pathogens. In addition, treatment of shrimp with the methyltransferase inhibitor 5-azacytidine resulted in upregulations of LDH and some protein processing genes, significant enrichment of S. algae, and simultaneous reduction of Vibrio in shrimp. Our results suggest that the colonization resistance can be memorized as epigenetic information by the host, which has played a pivotal role in vibriosis resistance. The findings of this study will aid in disease control and the selection of superior lines of shrimp with high disease resistance. Vibriosis is a bacterial disease that commonly occurs in animals, and causes high mortality and severe economic loss in aquaculture every year. Therefore, shaping a steady inherited resistance trait in organisms has received the highest priority in artificial selection. Whereas, the mechanisms underlying the development of such a resistance trait are mostly elusive. In this study, we found that penaeid shrimp can adopt a defense mechanism of colonization resistance against vibriosis. Wherein, a specific enrichment of a single probiotic species (Shewanella algae) in the intestine plays pivotal roles in reducing the Vibrio load and controlling vibriosis. Further evidence revealed that this process might be memorized and regulated by the host's epigenetic system. Activation of a subset of the host genes might provide proper niches for the enrichment of probiotics and simultaneous reduction of pathogens in the intestine through disruption of complete methylation. Together, our findings not only offer new insights into the key mechanisms in shaping disease resistance in shrimp, but also provide some clues for vibriosis control in aquaculture and for the selection of superior lines of shrimp with high disease resistance.
DOI	10.1371/journal.ppat.1012321
收录类别	SCI
语种	英语
资助项目	Natural Science Foundation of China[31830100] ; Natural Science Foundation of China[42176105] ; National Key Research & Development Program of China[2022YFD2400203] ; China Agriculture Research system-48 (Grant CARS-48) ; Taishan Scholars Program
WOS研究方向	Microbiology ; Parasitology ; Virology
WOS类目	Microbiology ; Parasitology ; Virology
WOS记录号	WOS:001272314400003
出版者	PUBLIC LIBRARY SCIENCE
WOS关键词	PACIFIC WHITE SHRIMP ; NECROSIS DISEASE AHPND ; LITOPENAEUS-VANNAMEI ; GUT MICROBIOTA ; TRANSCRIPTOME ANALYSIS ; DNA METHYLATION ; HOST ; HEPATOPANCREAS ; IMMUNITY ; STRATEGIES
引用统计
文献类型	期刊论文
条目标识符	http://ir.qdio.ac.cn/handle/337002/186255
专题	实验海洋生物学重点实验室
通讯作者	Li, Fuhua
作者单位	1.Chinese Acad Sci, Inst Oceanol, Ctr Ocean Mega Sci, CAS & Shandong Prov Key Lab Expt Marine Biol, Qingdao, Peoples R China 2.Chinese Acad Sci, Key Lab Breeding Biotechnol & Sustainable Aquacult, Wuhan, Peoples R China 3.Univ Chinese Acad Sci, Beijing, Peoples R China
第一作者单位	中国科学院海洋研究所
通讯作者单位	中国科学院海洋研究所
推荐引用方式 GB/T 7714	Yuan, Jianbo,Yu, Yang,Li, Shihao,et al. Shrimp shapes a resistance trait against vibriosis by memorizing the colonization resistance of intestinal microbiota[J]. PLOS PATHOGENS,2024,20(7):26.
APA	Yuan, Jianbo.,Yu, Yang.,Li, Shihao.,Zhang, Xiaojun.,Zhang, Chuntao.,...&Li, Fuhua.(2024).Shrimp shapes a resistance trait against vibriosis by memorizing the colonization resistance of intestinal microbiota.PLOS PATHOGENS,20(7),26.
MLA	Yuan, Jianbo,et al."Shrimp shapes a resistance trait against vibriosis by memorizing the colonization resistance of intestinal microbiota".PLOS PATHOGENS 20.7(2024):26.