Genome of the fatal tapeworm Sparganum proliferum uncovers mechanisms for cryptic life cycle and aberrant larval proliferation

Abstract

The cryptic parasite Sparganum proliferum proliferates in humans and invades tissues and organs. Only scattered cases have been reported, but S. proliferum infection is always fatal. However, S. proliferum’s phylogeny and life cycle remain enigmatic. To investigate the phylogenetic relationships between S. proliferum and other cestode species, and to examine the mechanisms underlying pathogenicity, we sequenced the entire genomes of S. proliferum and a closely related non–life-threatening tapeworm Spirometra erinaceieuropaei. Additionally, we performed larvae transcriptome analyses of S. proliferum plerocercoid to identify genes involved in asexual reproduction in the host. The genome sequences confirmed that the S. proliferum has experienced a clearly distinct evolutionary history from S. erinaceieuropaei. Moreover, we found that nonordinal extracellular matrix coordination allows asexual reproduction in the host, and loss of sexual maturity in S. proliferum are responsible for its fatal pathogenicity to humans. Our high-quality reference genome sequences should be valuable for future studies of pseudophyllidean tapeworm biology and parasitism.

Duplication and Losses of Opsin Genes in Lophotrochozoan Evolution

“…Interestingly, among the analyzed cestodes, a group of parasitic worms, only pseudophyllideans possess opsins, while cyclophyllideans, prevalently parasites of humans and terrestrial animals, do not ( fig. 2 ) ( Kikuchi et al 2021 ).…”

Complete sequencing of the mouse pseudoautosomal region, the most rapidly evolving ‘chromosome’

“…This is a long open-reading-frame (ORF) sequence (corresponding 275 amino acids in B6J) found in Mus species ( M. musculus and M. caroli NW_018388668.1). The identical sequence (VZI55075.1; SPRV2_LOCUS23037) was reported in the genome analysis of Sparganum proliferu [S9]; however, the genomic DNA of mice, which were the experimental host of the cryptic parasite, probably contaminated the parasite DNA sample. RNA-seq data showed the expression of the ORF sequence (Figure S3), but most EST clones showing significant homology are antisense sequences.…”

Duplication and losses of opsin genes in lophotrochozoan evolution

“…Modern bryozoans only retained xenopsins, while all platyhelminths only possess r-opsins and retinochromes, although it has been shown the expression of a xenopsin in larval eyes and ciliary structures (phaosomes) of polycladids, indicating that they were present in the platyhelminths common ancestor (Rawlinson et al 2019). Interestingly, among the analysed cestodes, a group of parasitic worms, only pseudophyllideans possess opsins, while cyclophyllideans, prevalently parasites of humans and domesticated animals, do not (Kikuchi et al 2021).…”