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DNA Barcoding of Flat Oyster Species Reveals the Presence of Ostrea

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DNA Barcoding of Flat Oyster Species Reveals the Presence of Ostrea Hamaguchi et al. Marine Biodiversity Records (2017) 10:4 DOI 10.1186/s41200-016-0105-7 RESEARCH Open Access DNA barcoding of flat oyster species reveals the presence of Ostrea stentina Payraudeau, 1826 (Bivalvia: Ostreidae) in Japan Masami Hamaguchi1*, Miyuki Manabe2, Naoto Kajihara1, Hiromori Shimabukuro1, Yuji Yamada3 and Eijiro Nishi4 Abstract Background: DNA barcoding is an effective method of accurately identifying morphologically similar oyster species. However, for some of Japan’s Ostrea species there are no molecular data in the international DNA databases. Methods: We sequenced the mitochondrial large subunit ribosomal DNA (LSrDNA) and cytochrome c oxidase subunit I (COI) gene of five known and two unidentified Ostrea species. Phylogenetic comparison with known Ostrea species permitted accurate species identification by DNA barcoding. Results: The molecular data, which were deposited in an international DNA database, allowed for a clear distinction among native Ostrea species in Japan. Moreover, the nucleotide sequence data confirmed that O. stentina (Atsuhime-gaki) inhabits Kemi and Ibusuki, Japan. Conclusions: This is the first record of O. stentina in Japan. These results provided for accurate species identification by DNA barcoding of the taxonomically problematic species O. futamiensis, O. fluctigera, O. setoensis and O. stentina in Japan. Keywords: Ostrea stentina, O. futamiensis, O. fluctigera, O. setoensis, DNA barcoding Background and many marine organisms have become endangered. Over the last half century, Japan’s coastal ecosystems Although many native and relict species of the last gla- have been severely damaged by human activity. The Seto cial epoch from the ancient East China Sea are found in Inland Sea, which is surrounded by the Japanese main the Seto Inland Sea (Botton et al. 1996; Futahashi 2011; islands of Honshu, Shikoku and Kyushu, is located in Hamaguchi et al. 2013), other invasive alien and indigen- the western part of Japan and is an area of human- ous species have been discovered where human activity induced ecological deterioration. The coastal areas were has led to the development of industrial areas along the reclaimed for urban and industrial use during a period coast (Iwasaki et al. 2004). Therefore, since 2008 we of rapid economic growth in the 1970s, leading to the have been conducting a long-term study to monitor ben- loss of 63.7% of the natural coast (tidal flats, seagrass thic species diversity at various tidal flats to promote the beds and estuary systems). Habitat loss, pollution, over- conservation of native marine fauna in the Seto Inland fishing, invasive species and now global climate change Sea and its adjacent marine areas supported by the are rapidly damaging the Seto Inland Sea. These factors Ministry of the Environment Monitoring Sites 1000 have gradually decreased the biodiversity of the area, Project and the Japan Long Term Ecological Research Network. We observed two morphologically different putative * Correspondence: [email protected] Ostrea species (Ostrea sp. A and Ostrea sp. B) during 1National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, 2-17-5 Maruishi, Hatsukaichi, Hiroshima 739-0452, the field surveys. The external features of Ostrea sp. A Japan were very similar to those of O. futamiensis Seki 1929 Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Hamaguchi et al. Marine Biodiversity Records (2017) 10:4 Page 2 of 10 while some morphological features were not identical. summarized claims made by other marine benthic re- We considered that Ostrea sp. A might be a juvenile searchers who maintain that O. futamiensis should not be form of another Ostrea species present in Japan. The ex- designated as near-threatened because O. futamiensis is ternal features of Ostrea sp. B were very similar to those possibly a junior synonym of O. denselamellosa. of Crassostrea gigas Thunberg, 1793 and we misidenti- Ostrea fluctigera Jousseume in Lamy, 1925 is a hard- fied the oyster as C. gigas at first. Some morphological to-find and taxonomically problematic species. The spe- features of Ostrea sp. B were similar to those of O. sten- cies is small and settles on hermit crab shells. Inaba and tina Payraudeau, 1826 but this species has not previously Torigoe (2004) re-classified the species and concluded been reported from Japan. Therefore, we performed ac- that O. deformis Lamarck, 1819 and Nanostrea exigua curate species identification of the oyster specimens. Harry 1985 were the synonyms of O. fluctigera. There In general, Ostreidae species are economically import- has only been one paper (Kuramochi 2007) published on ant marine organisms, but their morphological plasticity this topic since the reclassification by Inaba and Torigoe can cause taxonomic confusion. For example, shell (2004). morphology has been used as a primary feature to dis- Ostrea setoensis Habe 1957 is a small oyster and is also tinguish different species of oyster; however, the shell is a hard-to-find species in Japan. Habe (1957) described affected by habitat and environment (Tack et al. 1992; the oyster as O. sedea setoensis, which is a subspecies of Yamaguchi 1994; Lam and Morton 2004, 2006; Liu et al. O. sedea Iredale, 1939 from Australia. However, he later 2011). In recent years, molecular analyses have been transferred the oyster to the genus Neopycnodonte (Habe used to accurately identify Ostreidae species. Methods 1977). Torigoe (1983) claimed that it was an Ostrea spe- such as DNA barcoding (Hebert et al. 2003; Schindel cies based on its anatomy and shell morphology and and Miller 2005) have been used to detect hidden and considered it O. setoensis. cryptic species, determine their distributions, monitor As described above, species identification of O. futa- the biodiversity of marine fauna and reconstruct the miensis, O. fluctigera, O. setoensis, Ostrea sp. A and phylogeny of taxonomically confusing Ostrea species Ostrea sp. B by DNA barcoding has not been possible (Jozefowicz and O’Foighil 1998; Hurwood et al. 2005; until now because no nucleotide sequence data from Lapègue et al. 2006; Polson et al. 2009; Salvi et al. 2014). these oyster species has been deposited in international Moreover, DNA barcoding can be applied to all life DNA databases. stages of the oyster, e.g. planktonic larvae, spat and ju- In this study, we collected O. futamiensis, O. fluctigera venile forms. and Ostrea sp. A from the Seto Inland Sea, and other Five flat oyster species have been reported from Japan. Ostrea oysters including Ostrea sp. B and O. setoensis O. deselamellosa Lischke, 1869 and O. circumpicta from Japanese waters elesewhere. We analyzed the nu- Pilsbry, 1904 are fishery and aquaculture species utilized cleotide sequences of the mitochondrial large subunit in Japan. Molecular data of these two species have been ribosomal RNA (LSrRNA) and the cytochrome c oxidase deposited in the international DNA databases (DDBJ; subunit I (COI) gene to facilitate DNA barcoding of the DNA database of Japan/EMBL; European Molecular members of the genus Ostrea. Biology Laboratory/GenBank DNA database). The other three species recorded are small flat oysters, Methods viz. O. futamiensis, O. fluctigera Jousseume in Lamy, Sample collection and morphological identification of 1925 and O. setoensis Habe 1957 about which there is Ostrea species in Japan little taxonomical or ecological information. The mo- Ostrea sp. A and O. fluctigera specimens were sampled lecular data of these three species have not as yet been from the Kemi tidal flat in the Wakayama Prefecture. deposited in the international DNA databases. Ostrea sp. B were collected from Ibusuki in Kagoshima Ostrea futamiensis Seki 1929 was first discovered in Bay. Ostrea sp. B was settled onto polyvinyl chloride Futamigaura, Hyogo Prefecture, in the eastern part of plates used to culture Crassostrea nippona Seki, 1934 the Seto Inland Sea (Seki 1929). The oyster has a small oysters at the Kagoshima Prefectural Fisheries Technology (20–35 mm in length), moderately thick and irregularly and Development Center. O. futamiensis specimens were circular- or oval-shaped shell. The World Register of sampled from five tidal flats (Nakatsu, Oiso, Hishiwo, Marine Species (WoRMS; http://www.marinespecies.org/) Hinase and Kemi) in the Seto Inland Sea. O. setoensis lists O. futamiensis as a valid species. However, this species specimens were sampled from the Tamanoura tidal flat in is not commercially important in Japan, and thus eco- the Wakayama Prefecture. O. circumpicta and O. densela- logical and chorological research on this oyster is incom- mellosa were collected from the Yamagata and Kumamoto plete (Okutani 2000; Iijima 2007). Wada et al. (1996) Prefectures, Japan, respectively. All the oyster collection recommended that O. futamiensis be designated a sites are shown in Fig. 1 and Table 1. O. lurida Carpenter, near-threatened species. However, Henmi et al. (2014) 1864 was collected from Willapa Bay, Washington State, Hamaguchi et al. Marine Biodiversity Records (2017) 10:4 Page 3 of 10 DNA preparation All O. futamiensis, O. fluctigera and O. setoensis specimens were transported live to our laboratory in Hiroshima Prefecture, Japan. The adductor muscle of each individual organism was excised and preserved in 80% ethanol. The adductor muscle samples from O. cir- cumpicta, O. denselamellosa, Ostrea sp. A, Ostrea sp. B and O. lurida obtained from each sampling site were preserved in 80% ethanol until DNA extraction.
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