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

Taisei Kikuchi; Mehmet Dayi; Vicky L. Hunt; Kenji Ishiwata; Atsushi Toyoda; Asuka Kounosu; Simo Sun; Yasunobu Maeda; Yoko Kondo; Belkisyole Alarcon de Noya; Oscar Noya; Somei Kojima; Toshiaki Kuramochi; Haruhiko Maruyama

doi:10.1038/s42003-021-02160-8

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

Taisei Kikuchi, Mehmet Dayi, Vicky L. Hunt, Kenji Ishiwata, Atsushi Toyoda, Asuka Kounosu, Simo Sun, Yasunobu Maeda, Yoko Kondo, Belkisyole Alarcon de Noya, Oscar Noya, Somei Kojima, Toshiaki Kuramochi, Haruhiko Maruyama

Department of Life Sciences

Research output: Contribution to journal › Article › peer-review

8 Citations (SciVal)

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.

Original language	English
Article number	649
Journal	Communications Biology
Volume	4
Issue number	1
Early online date	31 May 2021
DOIs	https://doi.org/10.1038/s42003-021-02160-8
Publication status	Published - 31 Dec 2021

Bibliographical note

Funding Information:
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.

Publisher Copyright:
© 2021, The Author(s).

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Funding

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.

ASJC Scopus subject areas

Medicine (miscellaneous)
General Biochemistry,Genetics and Molecular Biology
General Agricultural and Biological Sciences

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Kikuchi, T., Dayi, M., Hunt, V. L., Ishiwata, K., Toyoda, A., Kounosu, A., Sun, S., Maeda, Y., Kondo, Y., de Noya, B. A., Noya, O., Kojima, S., Kuramochi, T., & Maruyama, H. (2021). Genome of the fatal tapeworm Sparganum proliferum uncovers mechanisms for cryptic life cycle and aberrant larval proliferation. Communications Biology, 4(1), Article 649. https://doi.org/10.1038/s42003-021-02160-8

Kikuchi, T, Dayi, M, Hunt, VL, Ishiwata, K, Toyoda, A, Kounosu, A, Sun, S, Maeda, Y, Kondo, Y, de Noya, BA, Noya, O, Kojima, S, Kuramochi, T & Maruyama, H 2021, 'Genome of the fatal tapeworm Sparganum proliferum uncovers mechanisms for cryptic life cycle and aberrant larval proliferation', Communications Biology, vol. 4, no. 1, 649. https://doi.org/10.1038/s42003-021-02160-8

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title = "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{\textquoteright}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.",

author = "Taisei Kikuchi and Mehmet Dayi and Hunt, {Vicky L.} and Kenji Ishiwata and Atsushi Toyoda and Asuka Kounosu and Simo Sun and Yasunobu Maeda and Yoko Kondo and {de Noya}, {Belkisyole Alarcon} and Oscar Noya and Somei Kojima and Toshiaki Kuramochi and Haruhiko Maruyama",

note = "Funding Information: 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. Publisher Copyright: {\textcopyright} 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

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AU - Toyoda, Atsushi

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AU - Sun, Simo

AU - Maeda, Yasunobu

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AU - de Noya, Belkisyole Alarcon

AU - Noya, Oscar

AU - Kojima, Somei

AU - Kuramochi, Toshiaki

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N2 - 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.

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

Abstract

Bibliographical note

Funding

ASJC Scopus subject areas

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