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Preliminary Application of Molecular Monitoring of the Pacific Herring (Clupea pallasii) Based on Real-time PCR Assay Utilization on Environmental Water Samples

  • Kim, Keun-Yong (Department of Genetic Analysis, AquaGenTech, Co., Ltd) ;
  • Heo, Jung Soo (Department of Genetic Analysis, AquaGenTech, Co., Ltd) ;
  • Moon, Seong Yong (South Sea Fisheries Research Institute, National Institute of Fisheries Science) ;
  • Kim, Keun-Sik (Fishes/Amphibians & Reptile Team, Research Center for Endangered Species, National Institute of Ecology) ;
  • Choi, Jung-Hwa (Jeju Fisheries Research Institute, National Institute of Fisheries Science) ;
  • Yoo, Joon-Taek (Cetacean Research Institute, National Institute of Fisheries Science)
  • Received : 2021.09.10
  • Accepted : 2021.09.13
  • Published : 2021.09.30

Abstract

Pacific herring, Clupea pallasii, a keystone species with significant ecological and commercial importance, is declining globally throughout much of its range. While traditional fishing equipment methods remain limited, new sensitive and rapid detection methods should be developed to monitor fisheries resources. To monitor the presence and quantity of C. pallasii from environmental DNA (eDNA) extracted from seawater samples, a pair of primers and a TaqMan® probe specific to this fish based on mitochondrial cytochrome b (COB) sequences were designed for the real-time PCR (qPCR) assay. The combination of our molecular markers showed high specificity in the qPCR assay, which affirmed the success of presenting a positive signal only in the C. pallasii specimens. The markers also showed a high sensitivity for detecting C. pallasii genomic DNA in the range of 1 pg~100 ng rxn-1 and its DNA plasmid containing COB amplicon in the range of 1~100,000copies rxn-1, which produced linear standard calibration curves (r2=0.99). We performed a qPCR assay for environmental water samples obtained from 29 sampling stations in the southeastern coastal regions of South Korea using molecular markers. The assay successfully detected the C. pallasii eDNA from 14 stations (48.2%), with the highest mean concentration in Jinhae Bay with a value of 76.09±18.39 pg L-1 (246.20±58.58 copies L-1). Our preliminary application of molecular monitoring of C. pallasii will provide essential information for efficient ecological control and management of this valuable fisheries resource.

Keywords

Acknowledgement

We sincerely appreciate Mr. Biet Thanh Tran of Pukyong National University for his valuable comments and suggestions, which helped us to improve the quality of the article.

References

  1. Asahida, T., T. Kobayashi, K. Saitoh and I. Nakayama. 1996. Tissue preservation and total DNA extraction form fish stored at ambient temperature using buffers containing high concentration of urea. Fisheries Science 62: 727-730. https://doi.org/10.2331/fishsci.62.727.
  2. Bylemans, J., E.M. Furlan, C.M. Hardy, P. McGuffie, M. Lintermans and D.M. Gleeson. 2017. An environmental DNA-based method for monitoring spawning activity: A case study, using the endangered Macquarie perch (Macquaria australasica). Methods in Ecology and Evolution 8: 646-655. https://doi.org/10.1111/2041-210X.12709.
  3. Collins, R.A., O.S. Wangensteen, E.J. O'Gorman, S. Mariani, D.W. Sims and M.J. Genner. 2018. Persistence of environmental DNA in marine systems. Communications Biology 1: 185. https://doi.org/10.1038/s42003-018-0192-6.
  4. Deepak, S.A., K.R. Kottapalli, R. Rakwal, G. Oros, K.S. Rangappa, H. Iwahashi, Y. Masuo and G.K. Agrawal. 2007. Real-time PCR: Revolutionizing detection and expression analysis of genes. Current Genomics 8: 234-251. https://doi.org/10.2174/138920207781386960.
  5. Espy, M.J., J.R. Uhl, L.M. Sloan, S.P. Buckwalter, M.F. Jones, E.A. Vetter, J.D.C. Yao, N.L. Wengenack, J.E. Rosenblatt, F.R. III Cockerill and T.F. Smith. 2006. Real-time PCR in clinical microbiology: Applications for routine laboratory testing. Clinical Microbiology Reviews 19: 165-256. https://doi.org/10.1128/CMR.19.1.165-256.2006.
  6. Ficetola, G.F., C. Miaud, F. Pompanon and P. Taberlet. 2008. Species detection using environmental DNA from water samples. Biology Letters 4: 423-425. https://doi.org/10.1098/rsbl.2008.0118.
  7. Grant, W.S., M. Liu, T. Gao and T. Yanagimoto. 2012. Limits of Bayesian skyline plot analysis of mtDNA sequences to infer historical demographies in Pacific herring (and other species). Molecular Phylogenetics and Evolution 65: 203-212. https://doi.org/10.1016/j.ympev.2012.06.006.
  8. Gwak, W.S. and A. Roy. 2021. Genetic diversity and population structure of Pacific herring Clupea pallasii in the Northeast Asia inferred from mtDNA marker. Ecological Genetics and Genomics 18: 100076. https://doi.org/10.1016/j.egg.2020.100076.
  9. Haegele, C.W. and J.F. Schweigert. 1985. Estimation of egg numbers in Pacific herring spawns on giant kelp. North American Journal of Fisheries Management 5: 65-71. https://doi.org/10.1577/1548-8659(1985)5<65:EOENIP>2.0.CO;2.
  10. Hall, T. 2011. BioEdit: An important software for molecular biology. GERF Bulletin of Bioscience 2: 60-61.
  11. Harada, A.E., E.A. Lindgren, M.C. Hermsmeier, P.A. Rogowski, E. Terrill and R.S. Burton. 2015. Monitoring spawning activity in a southern California marine protected area using molecular identification of fish eggs. PLOS ONE 10: e0134647. https://doi.org/10.1371/journal.pone.0134647.
  12. Hay, D.E., K.A. Rose, J. Schweigert and B.A. Megrey. 2008. Geographic variation in North Pacific herring populations: Pan-Pacific comparisons and implications for climate change impacts. Progress in Oceanography 77: 233-240. https://doi.org/10.1016/j.pocean.2008.03.015.
  13. Ji, H.S., D.W. Lee, J.H. Choi and K.H. Choi. 2015. Development of naturally spawned Pacific herring Clupea pallasii larvae. Korean Journal of Fisheries and Aquatic Sciences 48: 362-367 (in Korean). https://doi.org/10.5657/KFAS.2015.0362
  14. Katano, I., K. Harada, H. Doi, R. Souma and T. Minamoto. 2017. Environmental DNA method for estimating salamander distribution in headwater streams, and a comparison of water sampling methods. PLOS ONE 12: e0176541. https://doi.org/10.1371/journal.pone.0176541.
  15. Kitada, S., R. Yoshikai, T. Fujita, K. Hamasaki, R. Nakamichi and H. Kishino. 2017. Population structure and persistence of Pacific herring following the Great Tohoku earthquake. Conservation Genetics 18: 423-437. https://doi.org/10.1007/s10592-016-0918-2.
  16. Kochzius, M., C. Seidel, A. Antoniou, S.K. Botla, D. Campo, A. Cariani, E.G. Vazquez, J. Hauschild, C. Hervet, S. Hjorleifsdottir, G. Hreggvidsson, K. Kappel, M. Landi, A. Magoulas, V. Marteinsson, M. Nolte, S. Planes, F. Tinti, C. Turan, M.N. Venugopal, H. Weber and D. Blohm. 2010. Identifying fishes through DNA barcodes and microarrays. PLOS ONE 5: e12620. https://doi.org/10.1371/journal.pone.0012620.
  17. Lee, J.H., J.N. Kim, K. Nam, C.W. Kim and J.I. Kim. 2014. Distribution and species composition of larval fish during winter season in Jinhae Bay, Korea. Korean Journal of Ichthyology 26: 133-138.
  18. Lee, Y.D., J.H. Choi, S.Y. Moon, S.K. Lee and W.S. Gwak. 2017. Spawning characteristics of Clupea pallasii in the coastal waters off Gyeongnam, Korea, during spawning season. Ocean Science Journal 52: 581-586. https://doi.org/10.1007/s12601-017-0046-z.
  19. Li, H., S. Yang, Q. Tang, X. Zhou and Y. Sun. 2020. Long-term variation in the abundance of Pacific herring (Clupea pallasii) from the Yellow Sea in the western North Pacific and its relation to climate over the past 590 years. Fisheries Oceanography 29: 56-65. https://doi.org/10.1111/fog.12449.
  20. Li, X., X. Shen, X. Chen, D. Xiang, R.W. Murphy and Y. Shen. 2018. Detection of potential problematic cytb gene sequences of fishes in GenBank. Frontiers in Genetics 9: 30. https://doi.org/10.3389/fgene.2018.00030.
  21. Liu, J.X., A. Tatarenkov, T.D. Beacham, V. Gorbachev, S. Wildes and J.C. Avise. 2011. Effects of Pleistocene climatic fluctuations on the phylogeographic and demographic histories of Pacific herring (Clupea pallasii). Molecular Ecology 20: 3879-3893. https://doi.org/10.1111/j.1365-294X.2011.05213.x.
  22. McKechnie, I., D. Lepofsky, M.L. Moss, V.L. Butler, T.J. Orchard, G. Coupland, F. Foster, M. Caldwell and K. Lertzman. 2014. Archaeological data provide alternative hypotheses on Pacific herring (Clupea pallasii) distribution, abundance, and variability. Proceedings of the National Academy of Sciences of the United States of America 111: E807-E816. https://doi.org/10.1073/pnas.1316072111.
  23. Minamoto, T., K. Hayami, M.K. Sakata and A. Imamura. 2019. Real-time polymerase chain reaction assays for environmental DNA detection of three salmonid fish in Hokkaido, Japan: Application to winter surveys. Ecological Research 34: 237-242. https://doi.org/10.1111/1440-1703.1018.
  24. Moon, S.Y., J.H. Choi, H.W. Lee, J.N. Kim, J.S. Heo, W.S. Gwak and Y.D. Lee. 2019. Distribution and characteristics of Pacific herring Clupea pallasii spawning beds in Jinhae Bay, Korea. Korean Journal of Fisheries Aquatic Science 52: 534-538. https://doi.org/10.5657/KFAS.2019.0534.
  25. Moon, S.Y., J.H. Lee, J.H. Choi, H.S. Ji, J.T. Yoo, J.N. Kim and Y.J. Im. 2018. Seasonal variation of larval fish community in Jinhae Bay, Korea. Environmental Biology Research 36: 140-149. https://doi.org/10.11626/KJEB.2018.36.2.140
  26. Morita, S. 1985. History of the herring fishery and review of artificial propagation techiques for herring in Japan. Canadian Journal of Fisheries and Aquatic Sciences 42: s222-s229. https://doi.org/10.1139/f85-276.
  27. Okouchi, H., S. Yamane and M. Aritaki. 2008. Migration ecology of the herring Clupea pallasii after spawning in Miyako Bay and homing in the following year. Nippon Suisan Gakkaishi 74: 389-394. https://doi.org/10.2331/suisan.74.389
  28. Plough, L.V., M.B. Ogburn, C.L. Fitzgerald, R. Geranio, G.A. Marafino and K.D. Richie. 2018. Environmental DNA analysis of river herring in Chesapeake Bay: A powerful tool for monitoring threatened keystone species. PLOS ONE 13: e0205578. https://doi.org/10.1371/journal.pone.0205578.
  29. Port, J.A., J.L. O'Donnell, O.C. Romero-Maraccini, P.R. Leary, S.Y. Litvin, K.J. Nickols, K.M. Yamahara and R.P. Kelly. 2016. Assessing vertebrate biodiversity in a kelp forest ecosystem using environmental DNA. Molecular Ecology 25: 527-541. https://doi.org/10.1111/mec.13481.
  30. Sassoubre, L.M., K.M. Yamahara, L.D. Gardner, B.A. Block and A.B. Boehm. 2016. Quantification of environmental DNA (eDNA) shedding and decay rates for three marine fish. Environmental Science and Technology 50: 10456-10464. https://doi.org/10.1021/acs.est.6b03114.
  31. Shirafuji, N., T. Nakagawa, N. Murakami, S. Ito, T. Onitsuka, T. Morioka and Y. Watanabe. 2018. Successive use of different habitats during the early life stages of Pacific herring Clupea pallasii in Akkeshi waters on the east coast of Hokkaido. Fisheries Science 84: 227-236. https://doi.org/10.1007/s12562-018-1175-8.
  32. Stewart, K.A. 2019. Understanding the effects of biotic and abiotic factors on sources of aquatic environmental DNA. Biodiversity and Conservation 28: 983-1001. https://doi.org/10.1007/s10531-019-01709-8.
  33. Takahara, T., T. Minamoto, H. Yamanaka, H. Doi and Z.I. Kawabata. 2012. Estimation of fish biomass using environmental DNA. PLOS ONE 7: e35868. https://doi.org/10.1371/journal.pone.0035868.
  34. Takeuchi, A., T. Iijima, W. Kakuzen, S. Watanabe, Y. Yamada, A. Okamura, N. Horie, N. Mikawa, M.J. Miller, T. Kojima and K. Tsukamoto. 2019b. Release of eDNA by different life history stages and during spawning activities of laboratory-reared Japanese eels for interpretation of oceanic survey data. Scientific Reports 9: 6074. https://doi.org/10.1038/s41598-019-42641-9.
  35. Takeuchi, A., S. Watanabe, S. Yamamoto, M.J. Miller, T. Fukuba, T. Miwa, T. Okino, T. Minamoto and K. Tsukamoto. 2019a. First use of oceanic environmental DNA to study the spawning ecology of the Japanese eel Anguilla japonica. Marine Ecology Progress Series 609: 187-196. https://doi.org/10.3354/meps12828.
  36. Thomsen, P.F., J. Kielgast, L.L. Iversen, P.R. Moller, M. Rasmussen and E. Willerslev. 2012. Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLOS ONE 7: e41732. https://doi.org/10.1371/journal.pone.0041732.
  37. Thomsen, P.F. and E. Willerslev. 2015. Environmental DNA - An emerging tool in conservation for monitoring past and present biodiversity. Biological Conservation 183: 4-18. https://doi.org/10.1016/j.biocon.2014.11.019.
  38. Tomiyasu, M., H. Shirakawa, Y. Iino and K. Miyashita. 2018. Tracking migration of Pacific herring Clupea pallasii in a coastal spawning ground using acoustic telemetry. Fisheries Science 84: 79-89. https://doi.org/10.1007/s12562-017-1153-6.
  39. Watanabe, S., Y. Minegishi, T. Yoshinaga, J. Aoyama and K. Tsukamoto. 2004. A quick method for species identification of Japanese eel (Anguilla japonica) using real-time PCR: An onboard application for use during sampling surveys. Marine Biotechnology 6: 566-574. https://doi.org/10.1007/s10126-004-1000-5.
  40. Yamamoto, S., K. Minami, K. Fukaya, K. Takahashi, H. Sawada, H. Murakami, S. Tsuji, H. Hashizume, S. Kubonaga, T. Horiuchi, M. Hongo, J. Nishida, Y. Okugawa, A. Fujiwara, M. Fukuda, S. Hidaka, K.W. Suzuki, M. Miya, H. Araki, H. Yamanaka, A. Maruyama, K. Miyashita, R. Masuda, T. Minamoto and M. Kondoh. 2016. Environmental DNA as a 'snapshot' of fish distribution: A case study of Japanese Jack Mackerel in Maizuru Bay, Sea of Japan. PLOS ONE 11: e0149786. https://doi.org/10.1371/journal.pone.0149786.