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

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. Kikuchi et al. sequence the genome of the fatal tapeworm Sparganum proliferum and a closely related non-life-threatening tapeworm Spirometra erinaceieuropaei, and describe its genomic features suggesting the natural history and molecular mechanisms underlying pathogenicity. Their findings indicate that nonordinal extracellular matrix coordination is important for its asexual reproduction, and suggest that loss of sexual maturity contributes to the fatal pathogenicity of S. proliferum to humans.Japan Society for the Promotion of Science (JSPS) KAKENHIMinistry of Education, Culture, Sports, Science and Technology, Japan (MEXT)Japan Society for the Promotion of ScienceGrants-in-Aid for Scientific Research (KAKENHI) [26460510, 19H03212]; JST CRESTJapan Science & Technology Agency (JST)Core Research for Evolutional Science and Technology (CREST) [JPMJCR18S7]; AMED [18fk0108009h0003]Genome data analyses were partly performed using the DDBJ supercomputer system. We thank Ryusei Tanaka, Akemi Yoshida for assistance and comments. This work was supported by Japan Society for the Promotion of Science (JSPS) KAKENHI Grant Numbers 26460510 and 19H03212, AMED 18fk0108009h0003 and JST CREST Grant Number JPMJCR18S7.WOS:0006591242000012-s2.0-85107343266PubMed: 3405978