Transcriptome Responses to Different Environments in Intertidal Zones in the Peanut Worm Sipunculus nudus

SIMPLE SUMMARY: Sipunculus nudus is a species of significant economic importance because of its high nutritional and medicinal value. It is widely distributed along coastlines worldwide, particularly in China, where a comprehensive industry exists encompassing breeding, farming, processing, and sale. Traditionally, S. nudus is cultured on sandy beaches without the need for artificial diets. The organisms rely on nutrients from the surface sediment, including microalgae and other organic matter. These worms inhabit both the intertidal and subtidal zones, enduring varying immersion periods throughout their growth process. As a result, they are exposed to different abiotic factors, such as varying irradiation times, oxygen availability, and others. In our study, we investigated the transcriptomic response of S. nudus across high, middle, and low tidal flats. We analyzed and compared the differential gene expression and relevant metabolic pathways in S. nudus from different habitats. This analysis aimed to shed light on the molecular mechanisms underpinning physiological responses to diverse environments in burrowing species. Interestingly, we observed that the differential gene expression of S. nudus primarily involved metabolic pathways associated with disease and immune responses rather than thermal stress, calcification, and pH regulation. This finding highlights the close relationship between gene expression and S. nudus’ unique living habits ABSTRACT: The peanut worm (Sipunculus nudus) is an important intertidal species worldwide. Species living in the same aquaculture area might suffer different environmental impacts. To increase knowledge of the molecular mechanisms underlying the response to environmental fluctuations, we performed a transcriptome analysis of S. nudus from different intertidal zones using a combination of the SMRT platform and the Illumina sequencing platform. (1) A total of 105,259 unigenes were assembled, and 23,063 unigenes were perfectly annotated. The results of the PacBio Iso-Seq and IIIumina RNA-Seq enriched the genetic database of S. nudus. (2) A total of 830 DEGs were detected in S. nudus from the different groups. In particular, 33 DEGs had differential expression in the top nine KEGG pathways related to pathogens, protein synthesis, and cellular immune response and signaling. The results indicate that S. nudus from different zones experience different environmental stresses. (3) Several DEGs (HSPA1, NFKBIA, eEF1A, etc.) in pathways related to pathogens (influenza A, legionellosis, measles, and toxoplasmosis) had higher expression in groups M and L. HSPA1 was clearly enriched in most of the pathways, followed by NFKBIA. The results show that the peanut worms from the M and L tidal flats might have suffered more severe environmental conditions. (4) Some DEGs (MKP, MRAS, and HSPB1) were upregulated in peanut worms from the H tidal flat, and these DEGs were mainly involved in the MAPK signaling pathway. These results indicate that the MAPK pathway may play a vital role in the immune response of the peanut worm to the effects of different intertidal flats. This study provides a valuable starting point for further studies to elucidate the molecular basis of the response to different environmental stresses in S. nudus.