Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle

Takeshi Takeuchi; Ryo Koyanagi; Fuki Gyoja; Miyuki Kanda; Kanako Hisata; Manabu Fujie; Hiroki Goto; Shinichi Yamasaki; Kiyohito Nagai; Yoshiaki Morino; Hiroshi Miyamoto; Kazuyoshi Endo; Hirotoshi Endo; Hiromichi Nagasawa; Shigeharu Kinoshita; Shuichi Asakawa; Shugo Watabe; Noriyuki Satoh; Takeshi Kawashima

doi:10.1186/s40851-016-0039-2

Bivalve-specific gene expansion in the pearl oyster genome: implications of adaptation to a sessile lifestyle

Zoological Lett. 2016 Feb 18:2:3. doi: 10.1186/s40851-016-0039-2. eCollection 2016.

Authors

Takeshi Takeuchi¹, Ryo Koyanagi², Fuki Gyoja¹, Miyuki Kanda², Kanako Hisata¹, Manabu Fujie², Hiroki Goto², Shinichi Yamasaki², Kiyohito Nagai³, Yoshiaki Morino⁴, Hiroshi Miyamoto⁵, Kazuyoshi Endo⁶, Hirotoshi Endo⁷, Hiromichi Nagasawa⁸, Shigeharu Kinoshita⁹, Shuichi Asakawa⁹, Shugo Watabe¹⁰, Noriyuki Satoh¹, Takeshi Kawashima¹¹

Affiliations

¹ Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495 Japan.
² DNA Sequencing Section, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495 Japan.
³ Pearl Research Institute, Mikimoto CO. LTD, Shima, Mie 517-0403 Japan.
⁴ Graduate School of Life and Environmental Science, University of Tsukuba, Ibaraki, 305-8572 Japan.
⁵ Department of Genetic Engineering, Faculty of Biology-Oriented Science and Technology, Kinki University, 930 Nishimitani, Kinokawa, Wakayama 649-6493 Japan.
⁶ Department of Earth and Planetary Science, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033 Japan.
⁷ Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564 Japan.
⁸ Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657 Japan ; College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058 People's Republic of China.
⁹ Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657 Japan.
¹⁰ Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657 Japan ; Kitasato University School of Marine Bioscience, Sagamihara, Kanagawa 252-0373 Japan.
¹¹ Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495 Japan ; Present Address: Graduate School of Life and Environmental Science, University of Tsukuba, Ibaraki, 305-8572 Japan.

Abstract

Introduction: Bivalve molluscs have flourished in marine environments, and many species constitute important aquatic resources. Recently, whole genome sequences from two bivalves, the pearl oyster, Pinctada fucata, and the Pacific oyster, Crassostrea gigas, have been decoded, making it possible to compare genomic sequences among molluscs, and to explore general and lineage-specific genetic features and trends in bivalves. In order to improve the quality of sequence data for these purposes, we have updated the entire P. fucata genome assembly.

Results: We present a new genome assembly of the pearl oyster, Pinctada fucata (version 2.0). To update the assembly, we conducted additional sequencing, obtaining accumulated sequence data amounting to 193× the P. fucata genome. Sequence redundancy in contigs that was caused by heterozygosity was removed in silico, which significantly improved subsequent scaffolding. Gene model version 2.0 was generated with the aid of manual gene annotations supplied by the P. fucata research community. Comparison of mollusc and other bilaterian genomes shows that gene arrangements of Hox, ParaHox, and Wnt clusters in the P. fucata genome are similar to those of other molluscs. Like the Pacific oyster, P. fucata possesses many genes involved in environmental responses and in immune defense. Phylogenetic analyses of heat shock protein70 and C1q domain-containing protein families indicate that extensive expansion of genes occurred independently in each lineage. Several gene duplication events prior to the split between the pearl oyster and the Pacific oyster are also evident. In addition, a number of tandem duplications of genes that encode shell matrix proteins are also well characterized in the P. fucata genome.

Conclusions: Both the Pinctada and Crassostrea lineages have expanded specific gene families in a lineage-specific manner. Frequent duplication of genes responsible for shell formation in the P. fucata genome explains the diversity of mollusc shell structures. These duplications reveal dynamic genome evolution to forge the complex physiology that enables bivalves to employ a sessile lifestyle in the intertidal zone.

Keywords: Biomineralization; C1q; Genome; Heat shock proteins; Hox; ParaHox; Pearl oyster; Pinctada fucata.