Advertisement

Fisheries Science

, Volume 84, Issue 5, pp 837–848 | Cite as

Lineage specific detection of the scaly form of the pen shell Atrina spp. by a loop-mediated isothermal amplification method

  • Kazumasa HashimotoEmail author
  • Katsumasa Yamada
  • Akira Nagae
  • Yukihiko Matsuyama
Original Article Biology

Abstract

Taxonomy of the pen shell (genus Atrina) in East Asia has been confused because of the plasticity of the shell morphology and lack of unified morphological characteristics. We analyzed the mitochondrial cytochrome c oxidase subunit I (COI) sequence of the pen shell sampled from Ariake Bay and Seto Inland Sea, western Japan. All individuals were identified as the scaly form based on external morphology; however, their COI sequences were comprised of two distinct lineages. The sequence divergence between the two was 8.3%, indicating the high possibility that they are different species. The scaly form of the pen shell in Japan is one of the target species for resource enhancement, therefore COI lineage identification of broodstock individuals is critically important to avoid producing hybrid seed. We developed a loop-mediated isothermal amplification method that enables specific detection of the two lineages. This method can contribute to reducing the cost and time required for genotyping broodstock individuals prior to seed production.

Keywords

Pen shell Genotype identification LAMP 

Notes

Acknowledgements

We are indebted to Mr. Hirokazu Miyamoto, Mr. Tatsuhito Matoba and Mr. Munenori Hayashi who offered us bivalve samples. Mr. Hiroshi Aramaki kindly provided us with data of pen shell samples analyzed in Aramaki (2013). We would also like to express our gratitude to Drs. Kengo Suzuki, Takeo Kurihara and Takenori Sasaki for their useful suggestions. This work was supported by a grant from Japan Fisheries Research and Education Agency and Grants-in-Aid for Scientific Researches (Nos. 15K18731, 16K07859 and 18K11625) to K.H. and K.Y.

References

  1. Abbasi I, Kirstein OD, Hailu A, Warburg A (2016) Optimization of loop-mediated isothermal amplification (LAMP) assays for the detection of Leishmania DNA in human blood samples. Acta Trop 162:20–26CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aramaki H (2013) The relationship between an effect of DNA analysis and proportion of pen-shells, Atrina spp. in the innermost area of Ariake Bay. Bull Saga Prefect Ariake Fish Res Dev Cent 26:89–91 (in Japanese) Google Scholar
  3. Aramaki H, Ohkuma H (2011) Mortality of pen-shells, Atrina pectinata at the age of 1 in the Ariake sound off Saga Prefecture. Bull Saga Prefect Ariake Fish Res Dev Cent 25:1–7 (in Japanese) Google Scholar
  4. Barco A, Raupach MJ, Laakmann S, Neumann H, Knebelsberger T (2016) Identification of North Sea molluscs with DNA barcoding. Mol Ecol Resour 16:288–297.  https://doi.org/10.1111/1755-0998.12440 CrossRefPubMedGoogle Scholar
  5. Bennett KF, Reed AJ, Lutz RA (2011) DNA barcoding reveals Brachidontes (Bivalvia: Mytilidae) from two ecologically distinct intertidal habitats on Long Key, Florida Keys, are cryptic species, not ecotypes. Nautilus (Philadelphia). 125:63–71Google Scholar
  6. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  7. Enosawa M, Kageyama S, Sawai K, Watanabe K, Notomi T, Onoe S, Mori Y, Yokomizo Y (2003) Use of loop-mediated isothermal amplification of the IS900 sequence for rapid detection of cultured Mycobacterium avium subsp. paratuberculosis. J Clin Microbiol 41:4359–4365.  https://doi.org/10.1128/JCM.41.9.4359 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Fisheries Research Agency, Seikai National Fisheries Research Institute, National Research Institute of Fisheries and Environment of Inland Sea, Fukuoka Fisheries and Marine Technology Research Center, Saga Ariake Fisheries Promotion Center, Nagasaki Prefectural Institute of Fisheries (2015) Nimaigai Shigen Kinkyu Zosyoku Taisaku Itaku Jigyo Hokokusyo. Fisheries Agency (in Japanese) Google Scholar
  9. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  10. Fukuda S, Takao S, Kuwayama M, Shimazu Y, Miyazaki K (2006) Rapid detection of norovirus from fecal specimens by real-time reverse transcription-loop-mediated isothermal amplification assay. J Clin Microbiol 44:1376–1381.  https://doi.org/10.1128/JCM.44.4.1376 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321.  https://doi.org/10.1093/sysbio/syq010 CrossRefPubMedGoogle Scholar
  12. Habe T (1977) Systematics of Mollusca in Japan. Bivalvia and Scaphopoda. Hokuryukan, Tokyo (in Japanese) Google Scholar
  13. Hamamoto S, Takagi T (1985) Morphological characteristics of two bivalves, Atrina (Servatrina) pectinata (Linnaeus) and Tresus keenae (Kuroda et Habe), which inhabit in the sea area of Bisan Seto. Bull Kagawa Prefect Fish Exp Stn 1:25–36 (in Japanese) Google Scholar
  14. Hebert PDN, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54:852–859.  https://doi.org/10.1080/10635150500354886 CrossRefPubMedGoogle Scholar
  15. Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B 270:313–321.  https://doi.org/10.1098/rspb.2002.2218 CrossRefPubMedGoogle Scholar
  16. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2:e312.  https://doi.org/10.1371/journal.pbio.0020312 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Huber M (2010) Compendium of bivalves. ConchBooks, HackenheimGoogle Scholar
  18. Kawahara I, Ito S, Yamaguchi A (2004) Influence of the bullnose ray, Aetobatus flagellum, on the pen-shell, Atrina pectinata, in Ariake Sound. Bull Saga Prefect Ariake Fish Res Dev Cent 22:29–33 (in Japanese with English abstract) Google Scholar
  19. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120.  https://doi.org/10.1007/BF01731581 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Koga H (1992) Studies of pen-shells in the Ariake Sea—VI. Differences of form distinguished by texture of shell, and its distribution. Bull Saga Prefect Ariake Fish Res Dev Cent 14:9–24 (in Japanese with English abstract) Google Scholar
  21. Kuroda T, Habe T, Oyama K (1971) The sea shells of Sagami Bay. Maruzen Co., Ltd., TokyoGoogle Scholar
  22. Kurozumi T (2000) Pinnidae. In: Okutani T (ed) Marine mollusks in Japan. Tokai University Press, Tokyo, pp 886–889Google Scholar
  23. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948.  https://doi.org/10.1093/bioinformatics/btm404 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.  https://doi.org/10.1093/bioinformatics/btp187 CrossRefPubMedGoogle Scholar
  25. Lim KT, Teh CSJ, Thong KL (2013) Loop-mediated isothermal amplification assay for the rapid detection of Staphylococcus aureus. Biomed Res Int 2013:895816PubMedPubMedCentralGoogle Scholar
  26. Liu J, Li Q, Kong L, Yu H, Zheng X (2011a) Identifying the true oysters (Bivalvia: Ostreidae) with mitochondrial phylogeny and distance-based DNA barcoding. Mol Ecol Resour 11:820–830.  https://doi.org/10.1111/j.1755-0998.2011.03025.x CrossRefPubMedGoogle Scholar
  27. Liu J, Li Q, Kong L, Zheng X (2011b) Cryptic diversity in the pen shell Atrina pectinata (Bivalvia: Pinnidae): high divergence and hybridization revealed by molecular and morphological data. Mol Ecol 20:4332–4345.  https://doi.org/10.1111/j.1365-294X.2011.05275.x CrossRefPubMedGoogle Scholar
  28. Maeno Y, Suzuki K, Yurimoto T, Fuseya R, Kiyomoto S, Ohashi S, Oniki H (2009) Maturation process of broodstock of the pen shell Atrina pectinata (Linnaeus, 1767) in suspension culture. J Shellfish Res 28:561–568CrossRefGoogle Scholar
  29. Mikkelsen NT, Schander C, Willassen E (2007) Local scale DNA barcoding of bivalves (Mollusca): a case study. Zool Scr 36:455–463.  https://doi.org/10.1111/j.1463-6409.2006.00289.x CrossRefGoogle Scholar
  30. Min D-K, Lee J-S, Koh D-B, Je J-G (2004) Mollusks in Korea. Min Molluscan Research Institute, Seoul (in Korean)Google Scholar
  31. Mori Y, Notomi T (2009) Loop-mediated isothermal amplification (LAMP): a rapid, accurate, and cost-effective diagnostic method for infectious diseases. J Infect Chemother 15:62–69CrossRefPubMedGoogle Scholar
  32. Nagai S, Itakura S (2012) Specific detection of the toxic dinoflagellates Alexandrium tamarense and Alexandrium catenella from single vegetative cells by a loop-mediated isothermal amplification method. Mar Genomics 7:43–49.  https://doi.org/10.1016/j.margen.2012.03.001 CrossRefPubMedGoogle Scholar
  33. Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, Hase T (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28:E63CrossRefPubMedPubMedCentralGoogle Scholar
  34. Notomi T, Mori Y, Tomita N, Kanda H (2015) Loop-mediated isothermal amplification (LAMP): principle, features, and future prospects. J Microbiol 53:1–5.  https://doi.org/10.1007/612275-015-4656-V CrossRefPubMedGoogle Scholar
  35. Ohashi S, Fujii A, Oniki H, Osako K, Maeno Y, Yoshikoshi K (2008) The rearing of the pen shell Atrina pectinata larvae and juveniles (preliminary note). Aquac Sci 56:181–191 (in Japanese with English abstract) Google Scholar
  36. Okutani T (1997) Atrina (Servatrina) pectinata. In: Okiyama M et al (eds) Basic information on rare wild aquatic animals and plants in Japan (IV). Japan Fisheries Resource Conservation Association, Tokyo, pp 43–47 (in Japanese) Google Scholar
  37. Parida M, Posadas G, Inoue S, Hasebe F, Morita K (2004) Real-time reverse transcription loop-mediated isothermal amplification for rapid detection of West Nile virus. J Clin Microbiol 42:257–263.  https://doi.org/10.1128/JCM.42.1.257 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Rosewater J (1961) The family Pinnidae in the Indo-Pacific. Indo-Pacfic Mollusca 1:175–226Google Scholar
  39. Sakai M, Biswas G, Kono T, Hikima J, Yokoyama H (2015) Detection of Kudoa amamiensis using loop-mediated isothermal amplification (LAMP). Fish Pathol 50:119–122CrossRefGoogle Scholar
  40. Schultz PWW, Huber M (2013) Revision of the worldwide recent Pinnidae and some remarks on fossil European Pinnidae. Acta Conchyl 13:1–164Google Scholar
  41. Sekino M, Yamashita H (2016) Mitochondrial and nuclear DNA analyses of Saccostrea oysters in Japan highlight the confused taxonomy of the genus. J Molluscan Stud 82:492–506.  https://doi.org/10.1093/mollus/eyw022 CrossRefGoogle Scholar
  42. South Sea Mariculture Research Center (2010) Research and development on artificial seed production of comb pen shells, Atrina pectinata. National Fisheries Research & Development Institute (in Korean with English abstract) Google Scholar
  43. Wang M, Yu X, Yang S, Gui J (2000) A comparative study on isozyme phonotypic divergence among four types of pen shell Atrina pectinata Linnaeus. Trop Oceanol 19:45–50 (in Chinese with English abstract) Google Scholar
  44. Xu J, Zheng Q, Yu L, Liu R, Zhao X, Wang G, Wang Q, Cao J (2013) Loop-mediated isothermal amplification (LAMP) method for detection of genetically modified maize T25. Food Sci Nutr 1:432–438.  https://doi.org/10.1002/fsn3.68 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xue D, Wang H, Zhang T, Gao Y, Zhang S, Xu F (2012) Morphological and genetic identification of the validity of the species Atrina chinensis (Bivalvia: Pinnidae). J Shellfish Res 31:739–747.  https://doi.org/10.2983/035.031.0318 CrossRefGoogle Scholar
  46. Yokogawa K (1996) Genetic divergence in two forms of pen shell Atrina pectinata. Venus 55:25–39 (in Japanese with English abstract) Google Scholar
  47. Yu X, Mao Y, Wang M, Zhou L, Gui J (2004) Genetic heterogeneity analysis and RAPD marker detection among four forms of Atrina pectinata Linnaeus. J Shellfish Res 23:165–171Google Scholar
  48. Yurimoto T, Watanabe Y, Nasu H, Tobase N, Matsui S, Yoshioka N (2003) Relationship between environmental food and glycogen contents in pen shells. In: Sakai Y et al (eds) Aquaculture and pathobiology of crustacean and other species. Proceedings of the 32nd UJNR Aquaculture Panel Symposium. Santa Barbara, California, USA, pp 120–129Google Scholar
  49. Zheng Y, Yang A, Wu B, Sun X, Zhou L, Li D, Dong Y (2015) Studies on the spawning inducement and the conditions for the larval culture of Atrina pectinata. Prog Fish Sci 36:127–133.  https://doi.org/10.11758/yykxjz.20150619 (in Chinese with English abstract) CrossRefGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2018

Authors and Affiliations

  1. 1.Seikai National Fisheries Research InstituteNagasakiJapan
  2. 2.Center for Water Cycle, Marine Environment, and Disaster ManagementKumamoto UniversityKumamotoJapan

Personalised recommendations