Transcriptional profiles of the fish parasite Neoechinorhynchus agilis (Acanthocephala) emphasize energetic stress in males and high cell-division activity in females

Background: Thorny-headed worms (Acanthocephala) occur worldwide in gnathostome vertebrates feeding on mandibulate arthropods. They can manipulate host behavior, accumulate heavy metals, and have lately gained economic relevance as a pest in fish aquaculture. Yet, despite their ecological and economic significance, little is known about the gene-expressional background of acanthocephalan development, maturation, and reproduction in the definitive host. To fill this gap in knowledge, we studied Neoechinorhynchus agilis (Eoacanthocephala) specimens sampled from the digestive tracts of naturally infected thin-lipped mullets (Chelon ramada). Results: We generated a nuclear draft genome and a whole-body transcriptome assembly. Differential expression analysis based on transcript abundances of 36 males and 30 females revealed that 30% of the transcripts had sex-biased expression. Gene ontologies relating to energy metabolism and microtubules were enriched with male-biased genes; female-biased genes indicated increased cell division and transcription activity. Only 0.19% of genes were differentially expressed as a function of female size (using whole-body RNA weight as a proxy for size), versus 5.4% in males. Conclusions: Transcriptome annotations underlined energy metabolism and reproduction as major tasks in N. agilis life. Our results suggest that males, smaller than females and thus supposedly less competitive, struggle for sufficient energy to produce large quantities of sperm. Female-biased genes were consistent with the production and development of numerous eggs. Finally, we identified genes with particular importance in the growth or reproduction of N. agilis, that could be investigated as candidate targets for acanthocephalan control in fish aquaculture.