Transcriptomics reveals the temporal responses of sea cucumber (Apostichopus japonicus) to the challenge by bacterial...

Sea cucumber (Apostichopus japonicus) is of considerable commercial and ecological value, yet disease outbreaks substantially constrain the sustainable development of its aquaculture industry. The molecular mechanisms underlying A. japonicus's response to pathogenic bacterial invasion remain incompletely elucidated to date, particularly with respect to its differential response to peptidoglycans derived from distinct Gram-specific bacteria. In this study, the transcriptomes of A. japonicus coelomocytes were analyzed in response to challenges involving two different peptidoglycans: one from Gram-negative Escherichia coli (named "EK") and the other from Gram-positive Bacillus subtilis (named "BS"). Signal transduction, post-translational modification, and immune pathways were recognized as the dominant functions related to the identified transcripts. Significant variations in gene expression profiles were observed during the challenges, with tens of thousands of genes being expressed differently between the challenged and control groups. Further KEGG enrichment analyses revealed that the alternative complement pathway and apoptosis were the primary immune pathways, which were greatly up-regulated at 72 h after both challenges. Additionally, the enriched pathways revealed a distinct initial response of A. japonicus to different challenges, characterized by the upregulation of signal transduction pathways in the BS treatment group and stronger lipid and energy metabolism in the EK group. Furthermore, cell adhesion-related pathways were found to be enriched in A. japonicus at 96 h after the challenges. Moreover, according to the Venn diagram, the cytochrome c oxidase subunit I (CO1) and gag-pro-pol polyprotein transcripts were down-regulated throughout both challenges. Preliminary investigation of the function of the A. japonicus gag-pro-pol polyprotein was conducted using RNAi combined with RNA-Seq analysis. This revealed that four functional gene groups, including those responsible for vitamin transport, antioxidation and inflammation, cell adhesion, and complement activation, were positively regulated by this gene. Therefore, it can be speculated that the peptidoglycans from Gram-negative and -positive bacteria not only triggered differentiated immune reactions in A. japonicus, but also suppressed some immune response, nutrition absorption and energy delivery via the negative regulation of CO1 and gag-pro-pol polyprotein gene expression.