Transcriptomic analysis of oligochaete immune responses to myxosporeans infection: Branchiura sowerbyi infected with Myxobolus cultus

Yuanli Zhao; Xinhua Liu; Bingwen Xi; Qianqian Zhang; Aihua Li; Jinyong Zhang

doi:10.1016/j.jip.2019.107283

Transcriptomic analysis of oligochaete immune responses to myxosporeans infection: Branchiura sowerbyi infected with Myxobolus cultus

J Invertebr Pathol. 2020 Jan:169:107283. doi: 10.1016/j.jip.2019.107283. Epub 2019 Nov 22.

Authors

Yuanli Zhao¹, Xinhua Liu¹, Bingwen Xi², Qianqian Zhang¹, Aihua Li¹, Jinyong Zhang³

Affiliations

¹ Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture and State Key Laboratory of Freshwater Ecology and Biotechnology Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China.
² Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, 214081 Wuxi, China.
³ Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture and State Key Laboratory of Freshwater Ecology and Biotechnology Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: zhangjy@ihb.ac.cn.

PMID: 31765651
DOI: 10.1016/j.jip.2019.107283

Abstract

The Myxozoa are endoparasites characterized by a two-host life cycle that typically involves invertebrates and vertebrates as definitive and intermediate hosts, respectively. However, little is known about invertebrate-myxosporean interactions, particularly about patterns of host immune defense. We used RNA-sequencing to identify genes that are possibly involved in the immune responses of the oligochaete Branchiura sowerbyi naturally infected with Myxobolus cultus. De novo assembly of the B. sowerbyi transcriptome yielded 119,031 unigenes, with an average length of 896 bp and an N50 length of 1754 bp. Comparative transcriptome analysis revealed 4059 differentially expressed genes (DEGs) between M. cultus-infected and uninfected B. sowerbyi groups, including 3802 upregulated genes and 257 downregulated genes. Among the B. sowerbyi immune factors implicated in the responses to M. cultus infection, DEGs related to lectins, ubiquitin-mediated proteolysis, phagocytosis, oxidative-antioxidative responses, proteases, and protease inhibitors were upregulated. The expression of some immune-related molecules such as calmodulin, heat shock proteins, antimicrobial peptides, lysenin, and serum amyoid A protein were also significantly upregulated. The expression patterns of 14 immune-related DEGs identified by RNA-seq were validated by quantitative real-time polymerase chain reaction. This study is the first attempt to characterize the B. sowerbyi transcriptome and identify immune-related molecules possibly associated with M. cultus infection. It is also the first report of invertebrate host-myxosporean interactions at the transcriptomic level. Our results will facilitate the elucidation of adaptive evolution mechanisms of myxosporean parasites in the definitive host and the genetic basis for differences in resistance of invertebrate hosts of different genotypes to a myxosporean species.

Keywords: Branchiura sowerbyi; Innate immune response; Invertebrate-myxosporean interaction; Myxobolus cultus; Transcriptomics.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Gene Expression Profiling
Host-Parasite Interactions*
Immunity, Innate*
Myxobolus / physiology*
Oligochaeta / immunology*
Oligochaeta / parasitology