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    Particle Size Distribution of Environmental DNA from the Nuclei of Marine Fish
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    • Toshiaki Jo*
      Toshiaki Jo
      Graduate School of Human Development and Environment, Kobe University, 3-11 Tsurukabuto, Nada-ku, Kobe City, Hyogo 657-8501, Japan
      Research Fellow of Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo, 102-0083, Japan
      *Phone: +81-78-078-803-7743; e-mail: [email protected]
      More by Toshiaki Jo
      Orcidhttp://orcid.org/0000-0002-1138-9360
    • Mio Arimoto
      Mio Arimoto
      Faculty of Human Development, Kobe University, 3-11 Tsurukabuto, Nada-ku, Kobe City, Hyogo 657-8501, Japan
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    • Hiroaki Murakami
      Hiroaki Murakami
      Maizuru Fisheries Research Station, Field Science Education and Research Center, Kyoto University, Maizuru, Kyoto 625-0086, Japan
      More by Hiroaki Murakami
    • Reiji Masuda
      Reiji Masuda
      Maizuru Fisheries Research Station, Field Science Education and Research Center, Kyoto University, Maizuru, Kyoto 625-0086, Japan
      More by Reiji Masuda
    • Toshifumi Minamoto
      Toshifumi Minamoto
      Graduate School of Human Development and Environment, Kobe University, 3-11 Tsurukabuto, Nada-ku, Kobe City, Hyogo 657-8501, Japan
      More by Toshifumi Minamoto
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    Environmental Science & Technology

    Cite this: Environ. Sci. Technol. 2019, 53, 16, 9947–9956
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    https://doi.org/10.1021/acs.est.9b02833
    Published July 22, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    Environmental DNA (eDNA) analyses have enabled a more efficient surveillance of species distribution and composition than conventional methods. However, the characteristics and dynamics of eDNA (e.g., origin, state, transport, and fate) remain unknown. This is especially limited for the eDNA derived from nuclei (nu-eDNA), which has recently been used in eDNA analyses. Here, we compared the particle size distribution (PSD) of nu-eDNA from Japanese Jack Mackerel (Trachurus japonicus) with that of mt-eDNA (eDNA derived from mitochondria) reported in previous studies. We repeatedly sampled rearing water from the tanks under multiple temperatures and fish biomass levels, and quantified the copy numbers of size-fractioned nu-eDNA. We found that the concentration of nu-eDNA was higher than that of mt-eDNA at 3–10 μm size fraction. Moreover, at the 0.8–3 μm and 0.4–0.8 μm size fractions, eDNA concentrations of both types increased with higher temperature and their degradation tended to be suppressed. These results imply that the production of eDNA from large to small size fractions could buffer the degradation of small-sized eDNA, which could improve its persistence in water. Our findings will contribute to refine the difference between nu- and mt-eDNA properties, and assist eDNA analyses as an efficient tool for the conservation of aquatic species.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.9b02833.

    • Results of the particle size distributions of Japanese Jack Mackerel mt-eDNA at time bfr; results of the temporal changes of Japanese Jack Mackerel eDNA particle size distributions for each treatment level (PDF)

    • Raw values of eDNA concentrations (copies per 2 μL template DNA) in tank samples with nuclear DNA markers (XLSX)

    • Extended methodological details (PDF)

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    This article is cited by 52 publications.

    1. Eshani Hettiarachchi, Vicki H. Grassian. Impact of Surface Adsorption on DNA Structure and Stability: Implications for Environmental DNA Interactions with Iron Oxide Surfaces. Langmuir 2024, 40 (52) , 27194-27205. https://doi.org/10.1021/acs.langmuir.4c02501
    2. Pedro F..P. Brandão-Dias, Jennifer L. Tank, Elise D. Snyder, Ursula H. Mahl, Brett Peters, Diogo Bolster, Arial J. Shogren, Gary A. Lamberti, Kyle Bibby, Scott P. Egan. Suspended Materials Affect Particle Size Distribution and Removal of Environmental DNA in Flowing Waters. Environmental Science & Technology 2023, 57 (35) , 13161-13171. https://doi.org/10.1021/acs.est.3c02638
    3. Satsuki Tsuji, Hiroaki Murakami, Reiji Masuda. Analysis of the Persistence and Particle Size Distributional Shift of Sperm-Derived Environmental DNA to Monitor Jack Mackerel Spawning Activity. Environmental Science & Technology 2022, 56 (15) , 10754-10763. https://doi.org/10.1021/acs.est.2c01904
    4. Luke J. McCartin, Samuel A. Vohsen, Susan W. Ambrose, Michael Layden, Catherine S. McFadden, Erik E. Cordes, Jill M. McDermott, Santiago Herrera. Temperature Controls eDNA Persistence across Physicochemical Conditions in Seawater. Environmental Science & Technology 2022, 56 (12) , 8629-8639. https://doi.org/10.1021/acs.est.2c01672
    5. Matthew R. Charron, Matthew C. Yates, Daniel D. Heath. Stomach Content DNA ( scDNA ) Detection and Quantification for Predator Diet Assessment Using High‐Throughput Nanofluidic Chip Technology: Species‐Specific qPCR Assay Panel Development and Validation. Molecular Ecology Resources 2025, 22 https://doi.org/10.1111/1755-0998.14106
    6. Ryosuke Osawa, Toshiaki S. Jo, Risa Nakamura, Kyoko Futami, Tomoaki Itayama, Evans Asena Chadeka, Benard Ngetich, Sachiyo Nagi, Mihoko Kikuchi, Sammy M. Njenga, Collins Ouma, George O. Sonye, Shinjiro Hamano, Toshifumi Minamoto. Methodological assessment for efficient collection of Schistosoma mansoni environmental DNA and improved schistosomiasis surveillance in tropical wetlands. Acta Tropica 2024, 260 , 107402. https://doi.org/10.1016/j.actatropica.2024.107402
    7. Lingrui Li, Shouyu Zhang, Zhenhua Wang. eDNA technology reveals fish species diversity and ecological corridor function in large raft mussel aquaculture area in the East China Sea. Marine Pollution Bulletin 2024, 209 , 117171. https://doi.org/10.1016/j.marpolbul.2024.117171
    8. Toshiaki S. Jo, Yusuke Ozaki, Nao Matsuda, Hiroki Yamanaka. Assessment of Allometry in Environmental DNA and RNA Production From Ayu ( Plecoglossus altivelis ) in an Experimental Condition Using Mitochondrial and Nuclear Gene Markers. Environmental DNA 2024, 6 (6) https://doi.org/10.1002/edn3.70052
    9. Toshiaki S. Jo, Yoshiharu Sasaki. Evaluating the quantitative performance of environmental DNA metabarcoding for freshwater zooplankton community: a case study in Lake Biwa, Japan. Environmental Science and Pollution Research 2024, 31 (47) , 58069-58082. https://doi.org/10.1007/s11356-024-35025-8
    10. Jing Yang, Chao Li, Linus Shing Him Lo, Xu Zhang, Zhikui Chen, Jing Gao, Clara U, Zhijun Dai, Masahiro Nakaoka, Huayong Yang, Jinping Cheng. Artificial Intelligence-Assisted Environmental DNA Metabarcoding and High-Resolution Underwater Optical Imaging for Noninvasive and Innovative Marine Environmental Monitoring. Journal of Marine Science and Engineering 2024, 12 (10) , 1729. https://doi.org/10.3390/jmse12101729
    11. Héloïse Verdier, Thibault Datry, Maxime Logez, Lara Konecny‐Duprè, Maïlys Gauthier, Tristan Lefébure. Environmental DNA Particle Size Distribution and Quantity Differ Across Taxa and Organelles. Environmental DNA 2024, 6 (5) https://doi.org/10.1002/edn3.598
    12. Irmgard Sedlmayr, Tamara Schenekar. eDNA State and Medium Affect DNA Degradation Patterns in Seminatural Systems of Southern African Waterholes. Environmental DNA 2024, 6 (5) https://doi.org/10.1002/edn3.70025
    13. Marie Antony Dass, Craig D.H. Sherman, Roland A.H. van Oorschot, Kate Tuohey, Dadna Hartman, Gemma Carter, Annalisa Durdle. Assessing eDNA capture method from aquatic environment to optimise recovery of human mt-eDNA. Forensic Science International 2024, 361 , 112085. https://doi.org/10.1016/j.forsciint.2024.112085
    14. Zongwu Wei, Xuzhe Zhang, Yingzhan Chen, Hongjie Liu, Shaopeng Wang, Man Zhang, Honglin Ma, Kefu Yu, Liwei Wang. A new strategy based on a cascade amplification strategy biosensor for on-site eDNA detection and outbreak warning of crown-of-thorns starfish. Science of The Total Environment 2024, 927 , 172258. https://doi.org/10.1016/j.scitotenv.2024.172258
    15. Didier Pont. Predicting downstream transport distance of fish eDNA in lotic environments. Molecular Ecology Resources 2024, 24 (4) https://doi.org/10.1111/1755-0998.13934
    16. Toshiaki S. Jo. Larger particle size distribution of environmental RNA compared to environmental DNA: a case study targeting the mitochondrial cytochrome b gene in zebrafish (Danio rerio) using experimental aquariums. The Science of Nature 2024, 111 (2) https://doi.org/10.1007/s00114-024-01904-w
    17. Michelle Scriver, Ulla von Ammon, Cody Youngbull, Xavier Pochon, Jo-Ann L. Stanton, Neil J. Gemmell, Anastasija Zaiko. Drop it all: extraction-free detection of targeted marine species through optimized direct droplet digital PCR. PeerJ 2024, 12 , e16969. https://doi.org/10.7717/peerj.16969
    18. Elise D. Snyder, Jennifer L. Tank, Pedro F.P. Brandão-Dias, Kyle Bibby, Arial J. Shogren, Aaron W. Bivins, Brett Peters, Erik M. Curtis, Diogo Bolster, Scott P. Egan, Gary A. Lamberti. Environmental DNA (eDNA) removal rates in streams differ by particle size under varying substrate and light conditions. Science of The Total Environment 2023, 903 , 166469. https://doi.org/10.1016/j.scitotenv.2023.166469
    19. Toshiaki S. Jo. Factors affecting biphasic degradation of eDNA released by Japanese jack mackerel (Trachurus japonicus). Journal of Experimental Marine Biology and Ecology 2023, 568 , 151941. https://doi.org/10.1016/j.jembe.2023.151941
    20. Satsuki Tsuji, Hiroaki Murakami, Reiji Masuda. Assessing the potential of eDNA analysis for spawning surveys in marine environments: A case study on Japanese jack mackerel. 2023https://doi.org/10.1101/2023.09.10.557099
    21. Michelle Scriver, Anastasija Zaiko, Xavier Pochon, Ulla von Ammon. Harnessing decay rates for coastal marine biosecurity applications: A review of environmental DNA and RNA fate. Environmental DNA 2023, 5 (5) , 960-972. https://doi.org/10.1002/edn3.405
    22. Beilun Zhao, Peter M. van Bodegom, Krijn Baptist Trimbos. Bacterial abundance and pH associate with eDNA degradation in water from various aquatic ecosystems in a laboratory setting. Frontiers in Environmental Science 2023, 11 https://doi.org/10.3389/fenvs.2023.1025105
    23. Kara J. Andres, David M. Lodge, Suresh A. Sethi, Jose Andrés. Detecting and analysing intraspecific genetic variation with eDNA : From population genetics to species abundance. Molecular Ecology 2023, 32 (15) , 4118-4132. https://doi.org/10.1111/mec.17031
    24. Liwei Wang, Jiarong Xu, Hongjie Liu, Shaopeng Wang, Wenchao Ou, Man Zhang, Fen Wei, Songlin Luo, Biao Chen, Shaolong Zhang, Kefu Yu. Ultrasensitive and on-site eDNA detection for the monitoring of crown-of-thorns starfish densities at the pre-outbreak stage using an electrochemical biosensor. Biosensors and Bioelectronics 2023, 230 , 115265. https://doi.org/10.1016/j.bios.2023.115265
    25. Toshiaki S. Jo. Utilizing the state of environmental DNA (eDNA) to incorporate time-scale information into eDNA analysis. Proceedings of the Royal Society B: Biological Sciences 2023, 290 (1999) https://doi.org/10.1098/rspb.2023.0979
    26. Pedro F. P. Brandão‐Dias, Daniel M. C. Hallack, Elise D. Snyder, Jennifer L. Tank, Diogo Bolster, Sabrina Volponi, Arial J. Shogren, Gary A. Lamberti, Kyle Bibby, Scott P. Egan. Particle size influences decay rates of environmental DNA in aquatic systems. Molecular Ecology Resources 2023, 23 (4) , 756-770. https://doi.org/10.1111/1755-0998.13751
    27. Toshiaki S. Jo. A higher DNA damage rate in aqueous eDNA particles suggests intra‐cellular eDNA degradation in cellular environments. Environmental DNA 2023, 5 (2) , 343-349. https://doi.org/10.1002/edn3.383
    28. Songqian Huang, Kazutoshi Yoshitake, Shugo Watabe, Shuichi Asakawa. Environmental DNA study on aquatic ecosystem monitoring and management: Recent advances and prospects. Journal of Environmental Management 2022, 323 , 116310. https://doi.org/10.1016/j.jenvman.2022.116310
    29. Chipuriro Joseph, Mohammad Eshaq Faiq, Zhengyan Li, Gang Chen. Persistence and degradation dynamics of eDNA affected by environmental factors in aquatic ecosystems. Hydrobiologia 2022, 849 (19) , 4119-4133. https://doi.org/10.1007/s10750-022-04959-w
    30. Annette F. Govindarajan, Luke McCartin, Allan Adams, Elizabeth Allan, Abhimanyu Belani, Rene Francolini, Justin Fujii, Daniel Gomez-Ibañez, Amy Kukulya, Fredrick Marin, Kaitlyn Tradd, Dana R. Yoerger, Jill M. McDermott, Santiago Herrera. Improved biodiversity detection using a large-volume environmental DNA sampler with in situ filtration and implications for marine eDNA sampling strategies. Deep Sea Research Part I: Oceanographic Research Papers 2022, 189 , 103871. https://doi.org/10.1016/j.dsr.2022.103871
    31. Jie Wang, Ping Liu, Jiang Chang, Cheng Li, Feng Xie, Jianping Jiang, . Development of an eDNA metabarcoding tool for surveying the world’s largest amphibian. Current Zoology 2022, 68 (5) , 608-614. https://doi.org/10.1093/cz/zoab094
    32. Toshiaki Jo, Hiroki Yamanaka. Fine‐tuning the performance of abundance estimation based on environmental DNA ( eDNA ) focusing on eDNA particle size and marker length. Ecology and Evolution 2022, 12 (8) https://doi.org/10.1002/ece3.9234
    33. Toshiaki S. Jo, Kenji Tsuri, Hiroki Yamanaka. Can nuclear aquatic environmental DNA be a genetic marker for the accurate estimation of species abundance?. The Science of Nature 2022, 109 (4) https://doi.org/10.1007/s00114-022-01808-7
    34. Kotaro Sugawara, Yudai Sasaki, Kunihiro Okano, Miho Watanabe, Naoyuki Miyata. Application of eDNA for monitoring freshwater bivalve Nodularia nipponensis and its glochidium larvae. Environmental DNA 2022, 4 (4) , 908-919. https://doi.org/10.1002/edn3.304
    35. Toshifumi Minamoto. Environmental DNA analysis for macro-organisms: species distribution and more. DNA Research 2022, 29 (3) https://doi.org/10.1093/dnares/dsac018
    36. Yuan Lin, Jun Li, Zhenhua Wang, Shouyu Zhang, Kai Wang, Xunmeng Li. A Comparison of Fish Diversity in Rocky Reef Habitats by Multi-Mesh Gillnets and Environmental DNA Metabarcoding. Frontiers in Ecology and Evolution 2022, 10 https://doi.org/10.3389/fevo.2022.874558
    37. Satsuki Tsuji, Hiroaki Murakami, Reiji Masuda. Analysis of the persistence and particle size distributional shift of sperm-derived environmental DNA to monitor Jack Mackerel spawning activity. 2022https://doi.org/10.1101/2022.03.09.483695
    38. Toshiaki Jo, Kenta Takao, Toshifumi Minamoto. Linking the state of environmental DNA to its application for biomonitoring and stock assessment: Targeting mitochondrial/nuclear genes, and different DNA fragment lengths and particle sizes. Environmental DNA 2022, 4 (2) , 271-283. https://doi.org/10.1002/edn3.253
    39. Shawn Hinz, Jennifer Coston-Guarini, Michael Marnane, Jean-Marc Guarini. Evaluating eDNA for Use within Marine Environmental Impact Assessments. Journal of Marine Science and Engineering 2022, 10 (3) , 375. https://doi.org/10.3390/jmse10030375
    40. Yingchun Xing, Wanru Gao, Zhixin Shen, Yuanyuan Zhang, Jie Bai, Xingwei Cai, Jilong Ouyang, Yahui Zhao. A Review of Environmental DNA Field and Laboratory Protocols Applied in Fish Ecology and Environmental Health. Frontiers in Environmental Science 2022, 10 https://doi.org/10.3389/fenvs.2022.725360
    41. Annette F. Govindarajan, Luke McCartin, Allan Adams, Elizabeth Allan, Abhimanyu Belani, Rene Francolini, Justin Fujii, Daniel Gomez-Ibañez, Amy Kukulya, Fredrick Marin, Kaitlyn Tradd, Dana R. Yoerger, Jill M. McDermott, Santiago Herrera. Improved biodiversity detection using a large-volume environmental DNA sampler with in situ filtration and implications for marine eDNA sampling strategies. 2022https://doi.org/10.1101/2022.01.12.475892
    42. Nathaniel T. Marshall, Henry A. Vanderploeg, Subba Rao Chaganti. Environmental (e)RNA advances the reliability of eDNA by predicting its age. Scientific Reports 2021, 11 (1) https://doi.org/10.1038/s41598-021-82205-4
    43. Cindy Bessey, Simon Neil Jarman, Tiffany Simpson, Haylea Miller, Todd Stewart, John Kenneth Keesing, Oliver Berry. Passive eDNA collection enhances aquatic biodiversity analysis. Communications Biology 2021, 4 (1) https://doi.org/10.1038/s42003-021-01760-8
    44. Mathew Seymour, François K. Edwards, Bernard J. Cosby, Iliana Bista, Peter M. Scarlett, Francesca L. Brailsford, Helen C. Glanville, Mark de Bruyn, Gary R. Carvalho, Simon Creer. Environmental DNA provides higher resolution assessment of riverine biodiversity and ecosystem function via spatio-temporal nestedness and turnover partitioning. Communications Biology 2021, 4 (1) https://doi.org/10.1038/s42003-021-02031-2
    45. Matthew A. Barnes, Katy Klymus, Hiroki Yamanaka. Editorial: Environmental DNA Innovations for Conservation. Frontiers in Ecology and Evolution 2021, 9 https://doi.org/10.3389/fevo.2021.785077
    46. Toshiaki Jo, Masayuki K. Sakata, Hiroaki Murakami, Reiji Masuda, Toshifumi Minamoto. Universal performance of benzalkonium chloride for the preservation of environmental DNA in seawater samples. Limnology and Oceanography: Methods 2021, 19 (11) , 758-768. https://doi.org/10.1002/lom3.10459
    47. Mohan Amarasiri, Takashi Furukawa, Fumiyuki Nakajima, Kazunari Sei. Pathogens and disease vectors/hosts monitoring in aquatic environments: Potential of using eDNA/eRNA based approach. Science of The Total Environment 2021, 796 , 148810. https://doi.org/10.1016/j.scitotenv.2021.148810
    48. Beilun Zhao, Peter M. van Bodegom, Krijn Trimbos. The particle size distribution of environmental DNA varies with species and degradation. Science of The Total Environment 2021, 797 , 149175. https://doi.org/10.1016/j.scitotenv.2021.149175
    49. Robert T. R. Paine, Carla R. Hurt, Hayden T. Mattingly. Monitoring a minuscule madtom: Environmental DNA surveillance of the endangered pygmy madtom ( Noturus stanauli Etnier & Jenkins 1980) in the Duck and Clinch rivers, Tennessee. Environmental DNA 2021, 3 (4) , 745-759. https://doi.org/10.1002/edn3.179
    50. Toshiaki Jo, Toshifumi Minamoto. Complex interactions between environmental DNA (eDNA) state and water chemistries on eDNA persistence suggested by meta‐analyses. Molecular Ecology Resources 2021, 21 (5) , 1490-1503. https://doi.org/10.1111/1755-0998.13354
    51. Takaya Hirohara, Kenji Tsuri, Koichi Miyagawa, Robert T. R. Paine, Hiroki Yamanaka. The Application of PMA (Propidium Monoazide) to Different Target Sequence Lengths of Zebrafish eDNA: A New Approach Aimed Toward Improving Environmental DNA Ecology and Biological Surveillance. Frontiers in Ecology and Evolution 2021, 9 https://doi.org/10.3389/fevo.2021.632973
    52. Matthew A. Barnes, W. Lindsay Chadderton, Christopher L. Jerde, Andrew R. Mahon, Cameron R. Turner, David M. Lodge. Environmental conditions influence eDNA particle size distribution in aquatic systems. Environmental DNA 2021, 3 (3) , 643-653. https://doi.org/10.1002/edn3.160
    53. Christopher R. Troth, Alfred Burian, Quentin Mauvisseau, Mark Bulling, Jen Nightingale, Christophe Mauvisseau, Michael J. Sweet. Development and application of eDNA-based tools for the conservation of white-clawed crayfish. Science of The Total Environment 2020, 748 , 141394. https://doi.org/10.1016/j.scitotenv.2020.141394
    54. Toshiaki Jo, Hiroaki Murakami, Reiji Masuda, Toshifumi Minamoto. Selective collection of long fragments of environmental DNA using larger pore size filter. Science of The Total Environment 2020, 735 , 139462. https://doi.org/10.1016/j.scitotenv.2020.139462
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    Environmental Science & Technology

    Cite this: Environ. Sci. Technol. 2019, 53, 16, 9947–9956
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.est.9b02833
    Published July 22, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

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