Comparative transcriptomic analysis provided insights into the local molecular responses of swimming crabs, Portunus trituberculatus and mud crabs, Scylla paramamosain to the infection of Ameson portunus (Microsporidia)

Microsporidiosis has been increasingly causing severe economic losses in aquaculture. Insights into the molecular mechanism of host responses to aquatic microsporidia infection will be beneficial for the formulation of control strategies of microsporidiosis in aquaculture. Ameson portunus is the recently identified causative agent of toothpaste-like syndrome in Portunus trituberculatus and slurry-like syndrome in Scylla paramamosain. Here, muscle tissues of these two crabs at the early and late disease stages of A. portunus infection were subjected to the comparative transcriptomic analysis to disclose differential molecular responses of this microsporidian infection and characterize the host's responses dynamics against the infection at these two stages. These differentially expressed genes (DEGs) were mainly involved in DNA replication, metabolism, and immunity. Among them, the DEGs associated with DNA replication were significantly up-regulated, indicating that A. portunus can achieve proliferation by regulating the cellular responses of host. The significant upregulation of DEGs associated with recognizing and removing DNA damage, homologous recombination, and mismatch repair suggested that A. portunus damaged to the genetic material of crab muscle cells, and host repaired DNA damage caused by the infection of A. portunus by enhancing homologous recombination. The DEGs associated with amino acid and carbohydrate metabolism were significantly down-regulated, suggesting that muscle metabolic function was impaired in severely infected crabs, and energy supply, regulation of oxidative stress, and resistance to pathogens of host were significantly affected at the late disease stage. It could possibly explain why diseased P. trituberculatus and S. paramamosain exhibited reduced food intake, sluggish movement, and slow growth. In response to the infection, the two crabs exhibited different immune responses. P. trituberculatus responded to the infection of A. portunus by phagocytosis and apoptosis, and S. paramamosain induced cytokine production by recognizing the pathogen and signaling downstream to eventually clear the invading cells of A. portunus.

Automated summary

Microsporidiosis in aquaculture has caused severe economic losses. Understanding the molecular mechanism of host responses to aquatic microsporidia infection is important for controlling microsporidiosis. This study analyzed the transcriptome of muscle tissues from two crab species at different stages of Ameson portunus infection, revealing differential molecular responses and dynamic host responses. The findings suggested that A. portunus can regulate host cellular responses to achieve proliferation, and the infection causes DNA damage in host cells. Metabolic function and immune responses were significantly affected in severely infected crabs, leading to reduced food intake and slow growth. The two crab species exhibited different immune responses to A. portunus infection.