Skip to main content
SpringerLink
Log in

Advances in environmental DNA monitoring: standardization, automation, and emerging technologies in aquatic ecosystems

  • Review
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Environmental DNA (eDNA) monitoring, a rapidly advancing technique for assessing biodiversity and ecosystem health, offers a noninvasive approach for detecting and quantifying species from various environmental samples. In this review, a comprehensive overview of current eDNA collection and detection technologies is provided, emphasizing the necessity for standardization and automation in aquatic ecological monitoring. Furthermore, the intricacies of water bodies, from streams to the deep sea, and the associated challenges they pose for eDNA capture and analysis are explored. The paper delineates three primary eDNA survey methods, namely, bringing back water, bringing back filters, and bringing back data, each with specific advantages and constraints in terms of labor, transport, and data acquisition. Additionally, innovations in eDNA sampling equipment, including autonomous drones, subsurface samplers, and in-situ filtration devices, and their applications in monitoring diverse taxa are discussed. Moreover, recent advancements in species-specific detection and eDNA metabarcoding are addressed, highlighting the integration of novel techniques such as CRISPR-Cas and nanopore sequencing that enable precise and rapid detection of biodiversity. The implications of environmental RNA and epigenetic modifications are considered for future applications in providing nuanced ecological data. Lastly, the review stresses the critical role of standardization and automation in enhancing data consistency and comparability for robust long-term biomonitoring. We propose that the amalgamation of these technologies represents a paradigm shift in ecological monitoring, aligning with the urgent call for biodiversity conservation and sustainable management of aquatic ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Agarwal, P., and Singh, M.K. (2019). A multipurpose drone for water sampling & video surveillance. In: 2019 Second International Conference on Advanced Computational and Communication Paradigms (ICACCP). Gangtok.

  • Albers, C.N., Jensen, A., Bælum, J., and Jacobsen, C.S. (2013). Inhibition of DNA polymerases used in Q-PCR by structurally different soil-derived humic substances. Geomicrobiol J 30, 675–681.

    Article  CAS  Google Scholar 

  • Allison, M.J., Round, J.M., Bergman, L.C., Mirabzadeh, A., Allen, H., Weir, A., and Helbing, C.C. (2021). The effect of silica desiccation under different storage conditions on filter-immobilized environmental DNA. BMC Res Notes 14, 106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez, A.J., Khanna, M., Toranzos, G.A., and Stotzky, G. (1998). Amplification of DNA bound on clay minerals. Mol Ecol 7, 775–778.

    Article  CAS  Google Scholar 

  • Ames, C.L., Ohdera, A.H., Colston, S.M., Collins, A.G., Fitt, W.K., Morandini, A.C., Erickson, J.S., and Vora, G.J. (2021). Fieldable environmental DNA sequencing to assess jellyfish biodiversity in nearshore waters of the Florida Keys, United States. Front Mar Sci 8, 640527.

    Article  Google Scholar 

  • Anastasiadi, D., and Piferrer, F. (2020). A clockwork fish: Age prediction using DNA methylation-based biomarkers in the European seabass. Mol Ecol Resour 20, 387–397.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, S.R., and Thompson, L.R. (2022). Optimizing an enclosed bead beating extraction method for microbial and fish environmental DNA. Environ DNA 4, 291–303.

    Article  CAS  Google Scholar 

  • Andruszkiewicz, E.A., Starks, H.A., Chavez, F.P., Sassoubre, L.M., Block, B.A., and Boehm, A.B. (2017). Biomonitoring of marine vertebrates in Monterey Bay using eDNA metabarcoding. PLoS ONE 12, e0176343.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ariza, M., Fouks, B., Mauvisseau, Q., Halvorsen, R., Alsos, I.G., and de Boer, H.J. (2023). Plant biodiversity assessment through soil eDNA reflects temporal and local diversity. Methods Ecol Evol 14, 415–430.

    Article  Google Scholar 

  • Aw, J.G.A., Lim, S.W., Wang, J.X., Lambert, F.R.P., Tan, W.T., Shen, Y., Zhang, Y., Kaewsapsak, P., Li, C., Ng, S.B., et al. (2021). Determination of isoform-specific RNA structure with nanopore long reads. Nat Biotechnol 39, 336–346.

    Article  CAS  PubMed  Google Scholar 

  • Baerwald, M.R., Goodbla, A.M., Nagarajan, R.P., Gootenberg, J.S., Abudayyeh, O.O., Zhang, F., and Schreier, A.D. (2020). Rapid and accurate species identification for ecological studies and monitoring using CRISPR-based SHERLOCK. Mol Ecol Resour 20, 961–970.

    Article  PubMed  PubMed Central  Google Scholar 

  • Banerjee, B.P., Raval, S., Maslin, T.J., and Timms, W. (2018). Development of a UAV-mounted system for remotely collecting mine water samples. Int J Min Reclam Environ 34, 385–396.

    Article  Google Scholar 

  • Barnes, M.A., and Turner, C.R. (2016). The ecology of environmental DNA and implications for conservation genetics. Conserv Genet 17, 1–17.

    Article  CAS  Google Scholar 

  • Beemelmanns, A., Ribas, L., Anastasiadi, D., Moraleda-Prados, J., Zanuzzo, F.S., Rise, M.L., and Gamperl, A.K. (2021). DNA methylation dynamics in Atlantic salmon (Salmo salar) challenged with high temperature and moderate hypoxia. Front Mar Sci 7, 604878.

    Article  Google Scholar 

  • Bessey, C., Neil Jarman, S., Simpson, T., Miller, H., Stewart, T., Kenneth Keesing, J., and Berry, O. (2021). Passive eDNA collection enhances aquatic biodiversity analysis. Commun Biol 4, 236.

    Article  PubMed  PubMed Central  Google Scholar 

  • Biggs, J., Ewald, N., Valentini, A., Gaboriaud, C., Dejean, T., Griffiths, R.A., Foster, J., Wilkinson, J.W., Arnell, A., Brotherton, P., et al. (2015). Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus). Biol Conserv 183, 19–28.

    Article  Google Scholar 

  • Bista, I., Carvalho, G.R., Walsh, K., Seymour, M., Hajibabaei, M., Lallias, D., Christmas, M., and Creer, S. (2017). Annual time-series analysis of aqueous eDNA reveals ecologically relevant dynamics of lake ecosystem biodiversity. Nat Commun 8, 14087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowers, H., Pochon, X., von Ammon, U., Gemmell, N., Stanton, J.A., Jeunen, G.J., Sherman, C., and Zaiko, A. (2021). Towards the optimization of eDNA/eRNA sampling technologies for marine biosecurity surveillance. Water 13, 1113.

    Article  CAS  Google Scholar 

  • Breier, J.A., Jakuba, M.V., Saito, M.A., Dick, G.J., Grim, S.L., Chan, E.W., McIlvin, M. R., Moran, D.M., Alanis, B.A., Allen, A.E., et al. (2020). Revealing ocean-scale biochemical structure with a deep-diving vertical profiling autonomous vehicle. Sci Robot 5, eabc7104.

    Article  PubMed  Google Scholar 

  • Breier, J.A., Rauch, C.G., McCartney, K., Toner, B.M., Fakra, S.C., White, S.N., and German, C.R. (2009). A suspended-particle rosette multi-sampler for discrete biogeochemical sampling in low-particle-density waters. Deep Sea Res Part I Oceanogr Res Papers 56, 1579–1589.

    Article  CAS  Google Scholar 

  • Breier, J.A., Sheik, C.S., Gomez-Ibanez, D., Sayre-McCord, R.T., Sanger, R., Rauch, C., Coleman, M., Bennett, S.A., Cron, B.R., Li, M., et al. (2014). A large volume particulate and water multi-sampler with in situ preservation for microbial and biogeochemical studies. Deep Sea Res Part I Oceanogr Res Papers 94, 195–206.

    Article  CAS  Google Scholar 

  • Carraro, L., Hartikainen, H., Jokela, J., Bertuzzo, E., and Rinaldo, A. (2018). Estimating species distribution and abundance in river networks using environmental DNA. Proc Natl Acad Sci USA 115, 11724–11729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carvalho, C.S., de Oliveira, M.E., Rodriguez-Castro, K.G., Saranholi, B.H., and Galetti Jr, P.M. (2022). Efficiency of eDNA and iDNA in assessing vertebrate diversity and its abundance. Mol Ecol Resour 22, 1262–1273.

    Article  CAS  PubMed  Google Scholar 

  • Castendyk, D., Straight, B., Filiatreault, P., Thibeault, S., and Cameron, L. (2017). Aerial drones used to sample pit lake water reduce costs and improve safety. Mining Eng 69, 20–28.

    Google Scholar 

  • Chang, J.J.M., Ip, Y.C.A., Ng, C.S.L., and Huang, D. (2020). Takeaways from mobile DNA barcoding with BentoLab and MinION. Genes 11, 1121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, J., Zeng, H., Lv, W., Sun, N., Wang, C., Xu, W., Hu, M., Gan, X., He, L., He, S., et al. (2023). Pseudo-chromosome—length genome assembly for a deep-sea eel Ilyophis brunneus sheds light on the deep-sea adaptation. Sci China Life Sci 66, 1379–1391.

    Article  CAS  PubMed  Google Scholar 

  • Chen, X., Kong, Y., Zhang, S., Zhao, J., Li, S., and Yao, M. (2022). Comparative evaluation of common materials as passive samplers of environmental DNA. Environ Sci Technol 56, 10798–10807.

    Article  CAS  PubMed  Google Scholar 

  • Compton, J. (1991). Nucleic acid sequence-based amplification. Nature 350, 91–92.

    Article  CAS  PubMed  Google Scholar 

  • Coster, S.S., Dillon, M.N., Moore, W., and Merovich, G.T. (2021). The update and optimization of an eDNA assay to detect the invasive rusty crayfish (Faxonius rusticus). PLoS ONE 16, e0259084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Díaz-Abad, L., Bacco-Mannina, N., Madeira, F.M., Neiva, J., Aires, T., Serrao, E.A., Regalla, A., Patrício, A.R., and Frade, P.R. (2022). eDNA metabarcoding for diet analyses of green sea turtles (Chelonia mydas). Mar Biol 169, 18.

    Article  Google Scholar 

  • Díaz-Ferguson, E., Herod, J., Galvez, J., and Moyer, G. (2014). Development of molecular markers for eDNA detection of the invasive African jewelfish (Hemichromis letourneuxi): a new tool for monitoring aquatic invasive species in National Wildlife Refuges. MBI 5, 121–131.

    Article  Google Scholar 

  • Díaz, C., Wege, F.F., Tang, C.Q., Crampton-Platt, A., Rüdel, H., Eilebrecht, E., and Koschorreck, J. (2020). Aquatic suspended particulate matter as source of eDNA for fish metabarcoding. Sci Rep 10, 14352.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deiner, K., Bik, H.M., Mächler, E., Seymour, M., Lacoursière-Roussel, A., Altermatt, F., Creer, S., Bista, I., Lodge, D.M., de Vere, N., et al. (2017). Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Mol Ecol 26, 5872–5895.

    Article  PubMed  Google Scholar 

  • Den Uyl, P.A., Thompson, L.R., Errera, R.M., Birch, J.M., Preston, C.M., Ussler Iii, W., Yancey, C.E., Chaganti, S.R., Ruberg, S.A., Doucette, G.J., et al. (2022). Lake Erie field trials to advance autonomous monitoring of cyanobacterial harmful algal blooms. Front Mar Sci 9, 1021952.

    Article  Google Scholar 

  • Djurhuus, A., Port, J., Closek, C.J., Yamahara, K.M., Romero-Maraccini, O., Walz, K. R., Goldsmith, D.B., Michisaki, R., Breitbart, M., Boehm, A.B., et al. (2017). Evaluation of filtration and DNA extraction methods for environmental DNA biodiversity assessments across multiple trophic levels. Front Mar Sci 4, 314.

    Article  Google Scholar 

  • Doi, H., Akamatsu, Y., Watanabe, Y., Goto, M., Inui, R., Katano, I., Nagano, M., Takahara, T., and Minamoto, T. (2017). Water sampling for environmental DNA surveys by using an unmanned aerial vehicle. Limnol Ocean Methods 15, 939–944.

    Article  CAS  Google Scholar 

  • Doi, H., Takahara, T., Minamoto, T., Matsuhashi, S., Uchii, K., and Yamanaka, H. (2015a). Droplet digital polymerase chain reaction (PCR) outperforms real-time PCR in the detection of environmental DNA from an invasive fish species. Environ Sci Technol 49, 5601–5608.

    Article  CAS  PubMed  Google Scholar 

  • Doi, H., Uchii, K., Takahara, T., Matsuhashi, S., Yamanaka, H., and Minamoto, T. (2015b). Use of droplet digital PCR for estimation of fish abundance and biomass in environmental DNA surveys. PLoS ONE 10, e0122763.

    Article  PubMed  PubMed Central  Google Scholar 

  • Doi, H., Watanabe, T., Nishizawa, N., Saito, T., Nagata, H., Kameda, Y., Maki, N., Ikeda, K., and Fukuzawa, T. (2021). On-site environmental DNA detection of species using ultrarapid mobile PCR. Mol Ecol Resour 21, 2364–2368.

    Article  CAS  PubMed  Google Scholar 

  • Doyle, J., and Uthicke, S. (2021). Sensitive environmental DNA detection via lateral flow assay (dipstick)—A case study on corallivorous crown-of-thorns sea star (Acanthaster cf. solaris) detection. Environ DNA 3, 323–342.

    Article  CAS  Google Scholar 

  • Easson, C.G., Boswell, K.M., Tucker, N., Warren, J.D., and Lopez, J.V. (2020). Combined eDNA and acoustic analysis reflects diel vertical migration of mixed consortia in the gulf of Mexico. Front Mar Sci 7, 552.

    Article  Google Scholar 

  • Edwards, A., Soares, A., Debbonaire, A., and Edwards Rassner, S.M. (2022). Before you go: a packing list for portable DNA sequencing of microbiomes and metagenomes. Microbiology 168.

  • Egeter, B., Veríssimo, J., Lopes-Lima, M., Chaves, C., Pinto, J., Riccardi, N., Beja, P., and Fonseca, N.A. (2022). Speeding up the detection of invasive bivalve species using environmental DNA: A Nanopore and Illumina sequencing comparison. Mol Ecol Resour 22, 2232–2247.

    Article  CAS  PubMed  Google Scholar 

  • Elijah, O., Rahman, T.A., Leow, C.Y., Yeen, H.C., Sarijari, M.A., Aris, A., Salleh, J., and Chua, T.H. (2018). A concept paper on smart river monitoring system for sustainability in river. IJIE 10.

  • Enochs, I.C., Formel, N., Shea, L., Chomiak, L., Piggot, A., Kirkland, A., and Manzello, D. (2020). Subsurface automated samplers (SAS) for ocean acidification research. Bull Mar Sci 96, 735–752.

    Article  Google Scholar 

  • Evans, N.T., and Lamberti, G.A. (2018). Freshwater fisheries assessment using environmental DNA: a primer on the method, its potential, and shortcomings as a conservation tool. Fish Res 197, 60–66.

    Article  Google Scholar 

  • Everett, M.V., and Park, L.K. (2018). Exploring deep-water coral communities using environmental DNA. Deep Sea Res Part II Topic Stud Oceanogr 150, 229–241.

    Article  CAS  Google Scholar 

  • Fan, G., Song, Y., Yang, L., Huang, X., Zhang, S., Zhang, M., Yang, X., Chang, Y., Zhang, H., Li, Y., et al. (2020). Initial data release and announcement of the 10,000 Fish Genomes Project (Fish10K). Gigascience 9, giaa080.

    Article  PubMed  PubMed Central  Google Scholar 

  • Feng, C., Liu, R., Xu, W., Zhou, Y., Zhu, C., Liu, J., Wu, B., Li, Y., Qiu, Q., He, S., et al. (2021). The genome of a new anemone species (Actiniaria: Hormathiidae) provides insights into deep-sea adaptation. Deep Sea Res Part I Oceanogr Res Papers 170, 103492.

    Article  Google Scholar 

  • Feng, C., Wang, K., Xu, W., Yang, L., Wanghe, K., Sun, N., Wu, B., Wu, F., Yang, L., Qiu, Q., et al. (2023). Monsoon boosted radiation of the endemic East Asian carps. Sci China Life Sci 66, 563–578.

    Article  PubMed  Google Scholar 

  • Formel, N., Enochs, I.C., Sinigalliano, C., Anderson, S.R., and Thompson, L.R. (2021). Subsurface automated samplers for eDNA (SASe) for biological monitoring and research. HardwareX 10, e00239.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fries, D., Paul, J., Smith, M., Farmer, A., Casper, E., and Wilson, J. (2007). The autonomous microbial genosensor, an in situ sensor for marine microbe detection. Microsc Microanal 13, 514–515.

    Article  Google Scholar 

  • Fu, G.K., Hu, J., Wang, P.H., and Fodor, S.P.A. (2011). Counting individual DNA molecules by the stochastic attachment of diverse labels. Proc Natl Acad Sci USA 108, 9026–9031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fukuba, T., and Fujii, T. (2012). Microfabricated flow-through device for in situ gene analysis. In: Tiquia-Arashiro, S.M., ed. Molecular Biological Technologies for Ocean Sensing. Totowa: Humana Press. 59–72.

    Chapter  Google Scholar 

  • Fukuba, T., and Fujii, T. (2021). Lab-on-a-chip technology for in situ combined observations in oceanography. Lab Chip 21, 55–74.

    Article  CAS  PubMed  Google Scholar 

  • Fukuba, T., Goto, S., Wong, M.K.S., Minegishi, Y., Hyodo, S., Makabe-Kobayashi, Y., Sugai, Y., and Hamasaki, K. (2022). Development and evaluation of automated gene collector—ATGC-12S for environmental DNA sample archive at aquatic environments. In: OCEANS 2022. Hampton Roads. 1–5.

  • Fukuba, T., Miyaji, A., Okamoto, T., Yamamoto, T., Kaneda, S., and Fujii, T. (2011). Integrated in situ genetic analyzer for microbiology in extreme environments. RSC Adv 1, 1567–1573.

    Article  CAS  Google Scholar 

  • Gallo, N.D., James Cameron, N.D., Kevin Hardy, N.D., Patricia Fryer, N.D., Douglas H. Bartlett, N.D., and Lisa A. Levin, N.D. (2015). Submersible- and lander-observed community patterns in the Mariana and New Britain trenches: influence of productivity and depth on epibenthic and scavenging communities. Deep Sea Res Part I Oceanogr Res Papers 99, 119–133.

    Article  Google Scholar 

  • Gao, Z.M., Huang, J.M., Cui, G.J., Li, W.L., Li, J., Wei, Z.F., Chen, J., Xin, Y.Z., Cai, D.S., Zhang, A.Q., et al. (2019). In situ meta-omic insights into the community compositions and ecological roles of hadal microbes in the Mariana Trench. Environ Microbiol 21, 4092–4108.

    Article  CAS  PubMed  Google Scholar 

  • Gasparini, L., Crookes, S., Prosser, R.S., and Hanner, R. (2020). Detection of freshwater mussels (Unionidae) using environmental DNA in riverine systems. Environ DNA 2, 321–329.

    Article  Google Scholar 

  • Gilpatrick, T., Lee, I., Graham, J.E., Raimondeau, E., Bowen, R., Heron, A., Downs, B., Sukumar, S., Sedlazeck, F.J., and Timp, W. (2020). Targeted nanopore sequencing with Cas9-guided adapter ligation. Nat Biotechnol 38, 433–438.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Govindarajan, A.F., Francolini, R.D., Jech, J.M., Lavery, A.C., Llopiz, J.K., Wiebe, P.H., and Zhang, W.G. (2021). Exploring the use of environmental DNA (eDNA) to detect animal taxa in the mesopelagic zone. Front Ecol Evol 9, 574877.

    Article  Google Scholar 

  • Govindarajan, A.F., McCartin, L., Adams, A., Allan, E., Belani, A., Francolini, R., Fujii, J., Gomez-Ibañez, D., Kukulya, A., Marin, F., et al. (2022). Improved biodiversity detection using a large-volume environmental DNA sampler with in situ filtration and implications for marine eDNA sampling strategies. Deep Sea Res Part I Oceanogr Res Papers 189, 103871.

    Article  CAS  Google Scholar 

  • Graham, C.T., O’Connor, I., Broderick, L., Broderick, M., Jensen, O., and Lally, H.T. (2022). Drones can reliably, accurately and with high levels of precision, collect large volume water samples and physio-chemical data from lakes. Sci Total Environ 824, 153875.

    Article  CAS  PubMed  Google Scholar 

  • Grandy, J.J., Galpin, V., Singh, V., and Pawliszyn, J. (2020). Development of a drone-based thin-film solid-phase microextraction water sampler to facilitate on-site screening of environmental pollutants. Anal Chem 92, 12917–12924.

    Article  CAS  PubMed  Google Scholar 

  • Guatelli, J.C., Whitfield, K.M., Kwoh, D.Y., Barringer, K.J., Richman, D.D., and Gingeras, T.R. (1990). Isothermal, in vitro amplification of nucleic acids by a multienzyme reaction modeled after retroviral replication. Proc Natl Acad Sci USA 87, 1874–1878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halltech. (2019). OSMOS eDNA sampler. Ontario: Hall Tech Environmental and Aquatic Research Inc.

    Google Scholar 

  • Hannes, I.P., Mcnichols-O’rourke, K., Goguen, M., Fang, M., and Morris, T.J. (2021). Sampling protocol for the freshwater mussel Simpsonaias ambigua (Salamander Mussel) in Canada Canadian Technical Report of Fisheries and Aquatic Sciences 3411. Technical Report.

  • Hansen, B.K., Jacobsen, M.W., Middelboe, A.L., Preston, C.M., Marin Iii, R., Bekkevold, D., Knudsen, S.W., Møller, P.R., and Nielsen, E.E. (2020). Remote, autonomous real-time monitoring of environmental DNA from commercial fish. Sci Rep 10, 13272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison, J.B., Sunday, J.M., and Rogers, S.M. (2019). Predicting the fate of eDNA in the environment and implications for studying biodiversity. Proc R Soc B 286, 20191409.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison, J.G., John Calder, W., Shuman, B., and Alex Buerkle, C. (2021). The quest for absolute abundance: the use of internal standards for DNA-based community ecology. Mol Ecol Resour 21, 30–43.

    Article  PubMed  Google Scholar 

  • Hata, H., Ogasawara, K., and Yamashita, N. (2022). Population decline of an endangered unionid, Pronodularia japanensis, in streams is revealed by eDNA and conventional monitoring approaches. Hydrobiologia 849, 2635–2646.

    Article  Google Scholar 

  • Hendricks, A., Mackie, C.M., Luy, E., Sonnichsen, C.D., Miller, L.F., Wright, M., Grundke, I., Smith, J., Creelman, J.J., Tavasoli, M., et al. (2022). A Miniaturized and automated eDNA sampler: application to a marine environment. In: OCEANS 2022. Hampton Roads. 1–10.

  • Hendricks, A., Mackie, C.M., Luy, E., Sonnichsen, C., Smith, J., Grundke, I., Tavasoli, M., Furlong, A., Beiko, R.G., LaRoche, J., et al. (2023). Compact and automated eDNA sampler for in situ monitoring of marine environments. Sci Rep 13, 5210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herfort, L., Seaton, C., Wilkin, M., Roman, B., Preston, C.M., Marin Iii, R., Seitz, K., Smith, M.W., Haynes, V., Scholin, C.A., et al. (2016). Use of continuous, real-time observations and model simulations to achieve autonomous, adaptive sampling of microbial processes with a robotic sampler. Limnol Ocean Methods 14, 50–67.

    Article  Google Scholar 

  • Hoshino, T., and Inagaki, F. (2017). Application of stochastic labeling with random-sequence barcodes for simultaneous quantification and sequencing of environmental 16S rRNA genes. PLoS ONE 12, e0169431.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoshino, T., Nakao, R., Doi, H., and Minamoto, T. (2021). Simultaneous absolute quantification and sequencing of fish environmental DNA in a mesocosm by quantitative sequencing technique. Sci Rep 11, 4372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, Y., Wang, X., Xu, Y., Yang, H., Tong, Z., Tian, R., Xu, S., Yu, L., Guo, Y., Shi, P., et al. (2023). Molecular mechanisms of adaptive evolution in wild animals and plants. Sci China Life Sci 66, 453–495.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunter, M.E., Dorazio, R.M., Butterfield, J.S.S., Meigs-Friend, G., Nico, L.G., and Ferrante, J.A. (2017). Detection limits of quantitative and digital PCR assays and their influence in presence-absence surveys of environmental DNA. Mol Ecol Resour 17, 221–229.

    Article  CAS  PubMed  Google Scholar 

  • Igawa, T., Takahara, T., Lau, Q., and Komaki, S. (2019). An application of PCR-RFLP species identification assay for environmental DNA detection. PeerJ 7, e7597.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jakuba, M.V., Breier, J.A., Gomez-Ibanez, D., Tradd, K., and Saito, M.A. (2018). Clio: an autonomous vertical sampling vehicle for global ocean biogeochemical mapping. In: 2018 IEEE/OES Autonomous Underwater Vehicle Workshop (AUV). Porto. 1–8.

  • Jerde, C.L., and Mahon, A.R. (2015). Improving confidence in environmental DNA species detection. Mol Ecol Resour 15, 461–463.

    Article  PubMed  Google Scholar 

  • Jo, T.S. (2023). Methodological considerations for aqueous environmental RNA collection, preservation, and extraction. ANAL SCI 39, 1711–1718.

    Article  CAS  PubMed  Google Scholar 

  • Kagzi, K., Hechler, R.M., Fussmann, G.F., and Cristescu, M.E. (2022). Environmental RNA degrades more rapidly than environmental DNA across a broad range of pH conditions. Mol Ecol Resour 22, 2640–2650.

    Article  CAS  PubMed  Google Scholar 

  • Keller, B., and Willke, T. (2019). SnotBot: a whale of a deep-learning project. IEEE Spectr 56, 41–53.

    Article  Google Scholar 

  • Kelley, J.L., Tobler, M., Beck, D., Sadler-Riggleman, I., Quackenbush, C.R., Arias Rodriguez, L., and Skinner, M.K. (2021). Epigenetic inheritance of DNA methylation changes in fish living in hydrogen sulfide-rich springs. Proc Natl Acad Sci USA 118, e2014929118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirtane, A., Atkinson, J.D., and Sassoubre, L. (2020). Design and validation of passive environmental DNA samplers using granular activated carbon and montmorillonite clay. Environ Sci Technol 54, 11961–11970.

    Article  CAS  PubMed  Google Scholar 

  • Krehenwinkel, H., Pomerantz, A., Henderson, J.B., Kennedy, S.R., Lim, J.Y., Swamy, V., Shoobridge, J.D., Graham, N., Patel, N.H., Gillespie, R.G., et al. (2019a). Nanopore sequencing of long ribosomal DNA amplicons enables portable and simple biodiversity assessments with high phylogenetic resolution across broad taxonomic scale. Gigascience 8, giz006.

    Article  PubMed  PubMed Central  Google Scholar 

  • Krehenwinkel, Pomerantz, and Prost (2019b). Genetic biomonitoring and biodiversity assessment using portable sequencing technologies: current uses and future directions. Genes 10, 858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar, G., Farrell, E., Reaume, A.M., Eble, J.A., and Gaither, M.R. (2022). One size does not fit all: Tuning eDNA protocols for high- and low-turbidity water sampling. Environ DNA 4, 167–180.

    Article  CAS  Google Scholar 

  • Lally, H.T., O’Connor, I., Jensen, O.P., and Graham, C.T. (2019). Can drones be used to conduct water sampling in aquatic environments? A review. Sci Total Environ 670, 569–575.

    Article  CAS  PubMed  Google Scholar 

  • Lang, D., Wang, X., Liu, C., Geng, W., Irwin, D.M., Chen, S., Li, C., Yu, L., and Xiao, H. (2023). Birth-and-death evolution of ribonuclease 9 genes in Cetartiodactyla. Sci China Life Sci 66, 1170–1182.

    Article  CAS  PubMed  Google Scholar 

  • Laroche, O., Kersten, O., Smith, C.R., and Goetze, E. (2020). Environmental DNA surveys detect distinct metazoan communities across abyssal plains and seamounts in the western Clarion Clipperton Zone. Mol Ecol 29, 4588–4604.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, B., Zheng, L., Ye, J., Zhang, C., Zhou, J., Huang, Q., Guo, Y., Wang, L., Yu, P., Liu, S., et al. (2022a). CREB1 contributes colorectal cancer cell plasticity by regulating lncRNA CCAT1 and NF-κB pathways. Sci China Life Sci 65, 1481–1497.

    Article  CAS  PubMed  Google Scholar 

  • Li, G., Chen, X., Zhou, F., Liang, Y., Xiao, Y., Cao, X., Zhang, Z., Zhang, M., Wu, B., Yin, S., et al. (2021). Self-powered soft robot in the Mariana Trench. Nature 591, 66–71.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Xin, Y., Cai, D., Chen, J., Li, W., Wang, S.P., Wei, Z., and Zhang, A.Q. (2020). Development and scientific application of deep-sea multiple in situ nucleic acid collections (MISNAC) apparatus. In: Global Oceans 2020: Singapore-US Gulf Coast. Biloxi. 1–5.

  • Li, W., Qin, M., Hou, X., Zhang, J., Wang, S., Li, Y., Luo, Z., Deng, T., Song, T., Xu, C., et al. (2022b). Application of eDNA metabarcoding for detecting Anura in North China. Asian Herpetol Res 13, 224–231.

    Google Scholar 

  • Lisnerová, M., Holzer, A., Blabolil, P., and Fiala, I. (2023). Evaluation and optimization of an eDNA metabarcoding assay for detection of freshwater myxozoan communities. Environ DNA 5, 312–325.

    Article  Google Scholar 

  • Liu, G., Jin, Y., Peng, Y., Liu, D., and Wan, B. (2022). A novel active deep-sea low-damage pressure-retaining organisms sampler. Front Mar Sci 9, 1028052.

    Article  Google Scholar 

  • Liu, L., Wang, X., Zhao, W., Li, Q., Li, J., Chen, H., and Shan, G. (2023). Systematic characterization of small RNAs associated with C. elegans Argonautes. Sci China Life Sci 66, 1303–1322.

    Article  CAS  PubMed  Google Scholar 

  • Loeza-Quintana, T., Abbott, C.L., Heath, D.D., Bernatchez, L., and Hanner, R.H. (2020). Pathway to Increase Standards and Competency of eDNA Surveys (PISCeS) —Advancing collaboration and standardization efforts in the field of eDNA. Environ DNA 2, 255–260.

    Article  Google Scholar 

  • Madduppa, H., Cahyani, N.K.D., Anggoro, A.W., Subhan, B., Jefri, E., Sani, L.M.I., Arafat, D., Akbar, N., and Bengen, D.G. (2021). eDNA metabarcoding illuminates species diversity and composition of three phyla (chordata, mollusca and echinodermata) across Indonesian coral reefs. Biodivers Conserv 30, 3087–3114.

    Article  Google Scholar 

  • Maiello, G., Talarico, L., Carpentieri, P., De Angelis, F., Franceschini, S., Harper, L.R., Neave, E.F., Rickards, O., Sbrana, A., Shum, P., et al. (2022). Little samplers, big fleet: eDNA metabarcoding from commercial trawlers enhances ocean monitoring. Fisheries Res 249, 106259.

    Article  Google Scholar 

  • Majaneva, M., Diserud, O.H., Eagle, S.H.C., Boström, E., Hajibabaei, M., and Ekrem, T. (2018). Environmental DNA filtration techniques affect recovered biodiversity. Sci Rep 8, 4682.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall, N.T., Vanderploeg, H.A., and Chaganti, S.R. (2021). Environmental (e)RNA advances the reliability of eDNA by predicting its age. Sci Rep 11, 2769.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayne, B., Espinoza, T., Roberts, D., Butler, G.L., Brooks, S., Korbie, D., and Jarman, S. (2021). Nonlethal age estimation of three threatened fish species using DNA methylation: Australian lungfish, Murray cod and Mary River cod. Mol Ecol Resour 21, 2324–2332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCluskey, J., Flores, M.E., Hinojosa, J., Jafarzadeh, A., Moghadam, S.V., Phan, D.C., Green, R.T., and Kapoor, V. (2021). Tracking water with synthetic DNA tracers using droplet digital PCR. ACS EST Water 1, 1177–1183.

    Article  CAS  Google Scholar 

  • McKee, A.M., Spear, S.F., and Pierson, T.W. (2015). The effect of dilution and the use of a post-extraction nucleic acid purification column on the accuracy, precision, and inhibition of environmental DNA samples. Biol Conserv 183, 70–76.

    Article  Google Scholar 

  • McQuillan, J.S., and Robidart, J.C. (2017). Molecular-biological sensing in aquatic environments: recent developments and emerging capabilities. Curr Opin Biotechnol 45, 43–50.

    Article  CAS  PubMed  Google Scholar 

  • Miao, W., Song, L., Ba, S., Zhang, L., Guan, G., Zhang, Z., and Ning, K. (2020). Protist 10,000 Genomes Project. Innovation 1, 100058.

    PubMed  PubMed Central  Google Scholar 

  • Miaud, C., Arnal, V., Poulain, M., Valentini, A., and Dejean, T. (2019). eDNA increases the detectability of ranavirus infection in an alpine amphibian population. Viruses 11, 526.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minamoto, T., Fukuda, M., Katsuhara, K.R., Fujiwara, A., Hidaka, S., Yamamoto, S., Takahashi, K., and Masuda, R. (2017). Environmental DNA reflects spatial and temporal jellyfish distribution. PLoS ONE 12, e0173073.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miralles, L., Parrondo, M., Hernández de Rojas, A., Garcia-Vazquez, E., and Borrell, Y. J. (2019). Development and validation of eDNA markers for the detection of Crepidula fornicata in environmental samples. Mar Pollut Bull 146, 827–830.

    Article  CAS  PubMed  Google Scholar 

  • Miya, M., Sato, Y., Fukunaga, T., Sado, T., Poulsen, J.Y., Sato, K., Minamoto, T., Yamamoto, S., Yamanaka, H., Araki, H., et al. (2015). MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of more than 230 subtropical marine species. R Soc Open Sci 2, 150088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyata, K., Inoue, Y., Amano, Y., Nishioka, T., Yamane, M., Kawaguchi, T., Morita, O., and Honda, H. (2021). Fish environmental RNA enables precise ecological surveys with high positive predictivity. Ecol Indicat 128, 107796.

    Article  Google Scholar 

  • Moore, S.K., Mickett, J.B., Doucette, G.J., Adams, N.G., Mikulski, C.M., Birch, J.M., Roman, B., Michel-Hart, N., and Newton, J.A. (2021). An autonomous platform for near real-time surveillance of harmful algae and their toxins in dynamic coastal shelf environments. JMSE 9, 336.

    Article  Google Scholar 

  • Muñoz-Colmenero, M., Ardura, A., Clusa, L., Miralles, L., Gower, F., Zaiko, A., and Garcia-Vazquez, E. (2018). New specific molecular marker detects Ficopomatus enigmaticus from water eDNA before positive results of conventional sampling. J Nat Conserv 43, 173–178.

    Article  Google Scholar 

  • Mucciarone, D.A., DeJong, H.B., Dunbar, R.B., Takeshita, Y., Albright, R., and Mertz, K. (2021). Autonomous submersible multiport water sampler. HardwareX 9, e00197.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nathan, L.M., Simmons, M., Wegleitner, B.J., Jerde, C.L., and Mahon, A.R. (2014). Quantifying environmental DNA signals for aquatic invasive species across multiple detection platforms. Environ Sci Technol 48, 12800–12806.

    Article  CAS  PubMed  Google Scholar 

  • Nguyen, P.L., Sudheesh, P.S., Thomas, A.C., Sinnesael, M., Haman, K., and Cain, K.D. (2018). Rapid detection and monitoring of Flavobacterium psychrophilum in water by using a handheld, field-portable quantitative PCR system. J Aqua Anim Hlth 30, 302–311.

    Article  CAS  Google Scholar 

  • Nolan, K.P., Loeza-Quintana, T., Little, H.A., McLeod, J., Ranger, B., Borque, D.A., and Hanner, R.H. (2023). Detection of brook trout in spatiotemporally separate locations using validated eDNA technology. J Environ Stud Sci 13, 66–82.

    Article  Google Scholar 

  • Olins, H.C., Rogers, D.R., Preston, C., Ussler Iii, W., Pargett, D., Jensen, S., Roman, B., Birch, J.M., Scholin, C.A., Haroon, M.F., et al. (2017). Co-registered geochemistry and metatranscriptomics reveal unexpected distributions of microbial activity within a hydrothermal vent field. Front Microbiol 8, 1042.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ore, J., Elbaum, S., Burgin, A., and Detweiler, C. (2015). Autonomous aerial water sampling. J Field Robot 32, 1095–1113.

    Article  Google Scholar 

  • Ottesen, E.A. (2016). Probing the living ocean with ecogenomic sensors. Curr Opin Microbiol 31, 132–139.

    Article  PubMed  Google Scholar 

  • Ottesen, E.A., Young, C.R., Eppley, J.M., Ryan, J.P., Chavez, F.P., Scholin, C.A., and DeLong, E.F. (2013). Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc Natl Acad Sci USA 110, E488–E497.

    Google Scholar 

  • Pargett, D.M., Birch, J.M., Preston, C.M., Ryan, J.P., Zhang, Y., and Scholin, C.A. (2015). Development of a mobile ecogenomic sensor. In: OCEANS 2015 -MTS/IEEE Washington. Washington.

  • Patin, N.V., and Goodwin, K.D. (2023). Capturing marine microbiomes and environmental DNA: A field sampling guide. Front Microbiol 13, 1026596.

    Article  PubMed  PubMed Central  Google Scholar 

  • Paul, J., Scholin, C., van den Engh, G., and Perry, M.J. (2007). In situ instrumentation. Oceanography 20, 70–78.

    Article  Google Scholar 

  • Phelps, M. (2019). Increasing eDNA capabilities with CRISPR technology for real-time monitoring of ecosystem biodiversity. Mol Ecol Resour 19, 1103–1105.

    Article  CAS  PubMed  Google Scholar 

  • Pomerantz, A., Peñafiel, N., Arteaga, A., Bustamante, L., Pichardo, F., Coloma, L.A., Barrio-Amorós, C.L., Salazar-Valenzuela, D., and Prost, S. (2018). Real-time DNA barcoding in a rainforest using nanopore sequencing: opportunities for rapid biodiversity assessments and local capacity building. Gigascience 7.

  • Pomerantz, A., Sahlin, K., Vasiljevic, N., Seah, A., Lim, M., Humble, E., Kennedy, S., Krehenwinkel, H., Winter, S., Ogden, R., et al. (2022). Rapid in situ identification of biological specimens via DNA amplicon sequencing using miniaturized laboratory equipment. Nat Protoc 17, 1415–1443.

    Article  CAS  PubMed  Google Scholar 

  • Ponce, J.J., Arismendi, I., and Thomas, A. (2021). Using in-situ environmental DNA sampling to detect the invasive New Zealand Mud Snail (Potamopyrgus antipodarum) in freshwaters. PeerJ 9, e11835.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pope, K.L., Goldberg, C.S., Nelson, N.L., Cummings, A.K., Seaborn, T., and Piovia-Scott, J. (2020). Designing environmental DNA surveys in complex aquatic systems: Backpack sampling for rare amphibians in Sierra Nevada meadows. Aquat Conserv 30, 1975–1987.

    Article  Google Scholar 

  • Preston, C.M., Harris, A., Ryan, J.P., Roman, B., Marin, R., Jensen, S., Everlove, C., Birch, J., Dzenitis, J.M., Pargett, D., et al. (2011). Underwater application of quantitative PCR on an ocean mooring. PLoS ONE 6, e22522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian, S., Chen, Y., Xu, X., Peng, C., Wang, X., Wu, H., Liu, Y., Zhong, X., Xu, J., and Wu, J. (2022). Advances in amplification-free detection of nucleic acid: CRISPR/Cas system as a powerful tool. Anal Biochem 643, 114593.

    Article  CAS  PubMed  Google Scholar 

  • Rees, H.C., Maddison, B.C., Middleditch, D.J., Patmore, J.R.M., and Gough, K.C. (2014). REVIEW: The detection of aquatic animal species using environmental DNA—a review of eDNA as a survey tool in ecology. J Appl Ecol 51, 1450–1459.

    Article  CAS  Google Scholar 

  • Ribeiro, H., Martins, A., Gonçalves, M., Guedes, M., Tomasino, M.P., Dias, N., Dias, A., Mucha, A.P., Carvalho, M.F., Almeida, C.M.R., et al. (2019). Development of an autonomous biosampler to capture in situ aquatic microbiomes. PLoS ONE 14, e0216882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rishan, S.T., Kline, R.J., and Rahman, M.S. (2023). Applications of environmental DNA (eDNA) to detect subterranean and aquatic invasive species: A critical review on the challenges and limitations of eDNA metabarcoding. Environ Adv 12, 100370.

    Article  CAS  Google Scholar 

  • Robidart, J.C., Church, M.J., Ryan, J.P., Ascani, F., Wilson, S.T., Bombar, D., Marin Iii, R., Richards, K.J., Karl, D.M., Scholin, C.A., et al. (2014). Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean. ISME J 8, 1175–1185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robidart, J.C., Preston, C.M., Paerl, R.W., Turk, K.A., Mosier, A.C., Francis, C.A., Scholin, C.A., and Zehr, J.P. (2012). Seasonal Synechococcus and Thaumarchaeal population dynamics examined with high resolution with remote in situ instrumentation. ISME J 6, 513–523.

    Article  CAS  PubMed  Google Scholar 

  • Roman, B., Scholin, C., Jensen, S., Marin, R., Massion, E., and Feldman, J. (2005). The 2nd generation Environmental Sample Processor: Evolution of a robotic underwater biochemical laboratory. In: Proceedings of OCEANS 2005 MTS/IEEE. Washington.

  • Rourke, M.L., Fowler, A.M., Hughes, J.M., Broadhurst, M.K., DiBattista, J.D., Fielder, S., Wilkes Walburn, J., and Furlan, E.M. (2022). Environmental DNA (eDNA) as a tool for assessing fish biomass: a review of approaches and future considerations for resource surveys. Environ DNA 4, 9–33.

    Article  CAS  Google Scholar 

  • Ruan, H.T., Wang, R.L., Li, H.T., Liu, L., Kuang, T.X., Li, M., and Zou, K.S. (2022). Effects of sampling strategies and DNA extraction methods on eDNA metabarcoding: a case study of estuarine fish diversity monitoring. Zool Res 43, 192–204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saccò, M., Guzik, M.T., van der Heyde, M., Nevill, P., Cooper, S.J.B., Austin, A.D., Coates, P.J., Allentoft, M.E., and White, N.E. (2022). eDNA in subterranean ecosystems: applications, technical aspects, and future prospects. Sci Total Environ 820, 153223.

    Article  PubMed  Google Scholar 

  • Sato, M., Inoue, N., Nambu, R., Furuichi, N., Imaizumi, T., and Ushio, M. (2021). Quantitative assessment of multiple fish species around artificial reefs combining environmental DNA metabarcoding and acoustic survey. Sci Rep 11, 19477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schadewell, Y., and Adams, C.I.M. (2021). Forensics meets ecology—environmental DNA offers new capabilities for marine ecosystem and fisheries research. Front Mar Sci 8, 668822.

    Article  Google Scholar 

  • Schatz, M.C. (2017). Nanopore sequencing meets epigenetics. Nat Methods 14, 347–348.

    Article  CAS  PubMed  Google Scholar 

  • Schenekar, T. (2023). The current state of eDNA research in freshwater ecosystems: are we shifting from the developmental phase to standard application in biomonitoring? Hydrobiologia 850, 1263–1282.

    Article  Google Scholar 

  • Scholin, C., Birch, J., Jensen, S., Marin III, R., Massion, E., Pargett, D., Preston, C., Roman, B., and Ussler III, W. (2017). The quest to develop ecogenomic sensors: a 25-year history of the environmental sample processor (ESP) as a case study. Oceanography 30, 100–113.

    Article  Google Scholar 

  • Scholin, C., Doucette, G., Jensen, S., Roman, B., Pargett, D., Marin III, R., Preston, C., Jones, W., Feldman, J., Everlove, C., et al. (2009). Remote detection of marine microbes, small invertebrates, harmful algae, and biotoxins using the environmental sample processor (ESP). Oceanography 22, 158–167.

    Article  Google Scholar 

  • Seah, A., Lim, M.C.W., McAloose, D., Prost, S., and Seimon, T.A. (2020). MinION-based DNA barcoding of preserved and non-invasively collected wildlife samples. Genes 11, 445.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sepulveda, A.J., Birch, J.M., Barnhart, E.P., Merkes, C.M., Yamahara, K.M., Marin Iii, R., Kinsey, S.M., Wright, P.R., and Schmidt, C. (2020). Robotic environmental DNA bio-surveillance of freshwater health. Sci Rep 10, 14389.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sepulveda, A., Hutchins, P., Massengill, R., and Dunker, K. (2018). Tradeoffs of a portable, field-based environmental DNA platform for detecting invasive northern pike (Esox lucius) in Alaska. Manag Biol Inv 9, 253–258.

    Google Scholar 

  • Shaw, J.L.A., Weyrich, L.S., Hallegraeff, G., and Cooper, A. (2019). Retrospective eDNA assessment of potentially harmful algae in historical ship ballast tank and marine port sediments. Mol Ecol 28, 2476–2485.

    Article  CAS  PubMed  Google Scholar 

  • Shimoda, N., Izawa, T., Yoshizawa, A., Yokoi, H., Kikuchi, Y., and Hashimoto, N. (2014). Decrease in cytosine methylation at CpG island shores and increase in DNA fragmentation during zebrafish aging. AGE 36, 103–115.

    Article  CAS  PubMed  Google Scholar 

  • Shu, L., Ludwig, A., and Peng, Z. (2020). Standards for methods utilizing environmental DNA for detection of fish species. Genes 11, 296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sigsgaard, E.E., Jensen, M.R., Winkelmann, I.E., Møller, P.R., Hansen, M.M., and Thomsen, P.F. (2020). Population-level inferences from environmental DNA— Current status and future perspectives. Evol Appl 13, 245–262.

    Article  PubMed  Google Scholar 

  • Skinner, M., Murdoch, M., Loeza-Quintana, T., Crookes, S., and Hanner, R. (2020). A mesocosm comparison of laboratory-based and on-site eDNA solutions for detection and quantification of striped bass (Morone saxatilis) in marine ecosystems. Environ DNA 2, 298–308.

    Article  Google Scholar 

  • Smith, M.C., Bodrossy, L., and Craw, P. (2022). Chapter 6—Advances in in situ molecular systems for phytoplankton research and monitoring. In: Clementson, L. A., Eriksen, R.S., and Willis, A., eds. Advances in Phytoplankton Ecology. Amsterdam: Elsevier. 191–215.

    Chapter  Google Scholar 

  • Song, K., Brewer, A., Ahmadian, S., Shankar, A., Detweiler, C., and Burgin, A.J. (2017). Using unmanned aerial vehicles to sample aquatic ecosystems. Limnol Ocean Methods 15, 1021–1030.

    Article  Google Scholar 

  • Srivathsan, A., Lee, L., Katoh, K., Hartop, E., Kutty, S.N., Wong, J., Yeo, D., and Meier, R. (2021). ONTbarcoder and MinION barcodes aid biodiversity discovery and identification by everyone, for everyone. BMC Biol 19, 217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stat, M., Huggett, M.J., Bernasconi, R., DiBattista, J.D., Berry, T.E., Newman, S.J., Harvey, E.S., and Bunce, M. (2017). Ecosystem biomonitoring with eDNA: metabarcoding across the tree of life in a tropical marine environment. Sci Rep 7, 12240.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stern, R.F., Picard, K.T., Hamilton, K.M., Walne, A., Tarran, G.A., Mills, D., McQuatters-Gollop, A., and Edwards, M. (2015). Novel lineage patterns from an automated water sampler to probe marine microbial biodiversity with ships of opportunity. Prog Oceanogr 137, 409–420.

    Article  Google Scholar 

  • Taberlet, P., Coissac, E., Hajibabaei, M., and Rieseberg, L.H. (2012). Environmental DNA. Mol Ecol 21, 1789–1793.

    Article  CAS  PubMed  Google Scholar 

  • Takasaki, K., Aihara, H., Imanaka, T., Matsudaira, T., Tsukahara, K., Usui, A., Osaki, S., and Doi, H. (2021). Water pre-filtration methods to improve environmental DNA detection by real-time PCR and metabarcoding. PLoS ONE 16, e0250162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theissinger, K., Fernandes, C., Formenti, G., Bista, I., Berg, P.R., Bleidorn, C., Bombarely, A., Crottini, A., Gallo, G.R., Godoy, J.A., et al. (2023). How genomics can help biodiversity conservation. Trends Genet 39, 545–559.

    Article  CAS  PubMed  Google Scholar 

  • Thomas, A.C., Howard, J., Nguyen, P.L., Seimon, T.A., and Goldberg, C.S. (2018). eDNA Sampler: A fully integrated environmental DNA sampling system. Methods Ecol Evol 9, 1379–1385.

    Article  Google Scholar 

  • Thomas, A.C., Nguyen, P.L., Howard, J., and Goldberg, C.S. (2019). A self-preserving, partially biodegradable eDNA filter. Methods Ecol Evol 10, 1136–1141.

    Article  Google Scholar 

  • Thomas, A.C., Tank, S., Nguyen, P.L., Ponce, J., Sinnesael, M., and Goldberg, C.S. (2020). A system for rapid eDNA detection of aquatic invasive species. Environ DNA 2, 261–270.

    Article  Google Scholar 

  • Thomsen, P.F., and Willerslev, E. (2015). Environmental DNA - An emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183, 4–18.

    Article  Google Scholar 

  • Trembanis, A.C., Cary, C., Schmidt, V.E., Clarke, D., Crees, T., and Jackson, E. (2012). Modular autonomous biosampler (MAB)—A prototype system for distinct biological size-class sampling and preservation. In: 2012 Oceans. Hampton Roads. 1–6.

  • Truelove, N.K., Andruszkiewicz, E.A., and Block, B.A. (2019). A rapid environmental DNA method for detecting white sharks in the open ocean. Methods Ecol Evol 10, 1128–1135.

    Article  Google Scholar 

  • Truelove, N.K., Patin, N.V., Min, M., Pitz, K.J., Preston, C.M., Yamahara, K.M., Zhang, Y., Raanan, B.Y., Kieft, B., Hobson, B., et al. (2022). Expanding the temporal and spatial scales of environmental DNA research with autonomous sampling. Environ DNA 4, 972–984.

    Article  CAS  Google Scholar 

  • Tsuji, S., Iguchi, Y., Shibata, N., Teramura, I., Kitagawa, T., and Yamanaka, H. (2018). Real-time multiplex PCR for simultaneous detection of multiple species from environmental DNA: an application on two Japanese medaka species. Sci Rep 8, 9138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsuji, S., Takahara, T., Doi, H., Shibata, N., and Yamanaka, H. (2019). The detection of aquatic macroorganisms using environmental DNA analysis—a review of methods for collection, extraction, and detection. Environ DNA 1, 99–108.

    Article  Google Scholar 

  • Ushio, M. (2019). Use of a filter cartridge combined with intra-cartridge bead-beating improves detection of microbial DNA from water samples. Methods Ecol Evol 10, 1142–1156.

    Article  Google Scholar 

  • Ushio, M., Murakami, H., Masuda, R., Sado, T., Miya, M., Sakurai, S., Yamanaka, H., Minamoto, T., and Kondoh, M. (2017). Quantitative monitoring of multispecies fish environmental DNA using high-throughput sequencing. bioRxiv, 10.1101/113472.

  • Ussler, W., Preston, C., Tavormina, P., Pargett, D., Jensen, S., Roman, B., Marin Roman, I., Shah, S.R., Girguis, P.R., Birch, J.M., et al. (2013). Autonomous application of quantitative PCR in the deep sea: in situ surveys of aerobic methanotrophs using the deep-sea environmental sample processor. Environ Sci Technol 47, 9339–9346.

    Article  CAS  PubMed  Google Scholar 

  • Uthicke, S., Lamare, M., and Doyle, J.R. (2018). eDNA detection of corallivorous seastar (Acanthaster cf. solaris) outbreaks on the Great Barrier Reef using digital droplet PCR. Coral Reefs 37, 1229–1239.

    Article  Google Scholar 

  • Vélez-Nicolás, M., García-López, S., Barbero, L., Ruiz-Ortiz, V., and Sánchez-Bellón, Á. (2021). Applications of unmanned aerial systems (UASs) in hydrology: A review. Remote Sens 13, 1359.

    Article  Google Scholar 

  • Valsecchi, E., Coppola, E., Pires, R., Parmegiani, A., Casiraghi, M., Galli, P., and Bruno, A. (2022). A species-specific qPCR assay provides novel insight into range expansion of the Mediterranean monk seal (Monachus monachus) by means of eDNA analysis. Biodivers Conserv 31, 1175–1196.

    Article  Google Scholar 

  • van Dijk, E.L., Jaszczyszyn, Y., Naquin, D., and Thermes, C. (2018). The third revolution in sequencing technology. Trends Genet 34, 666–681.

    Article  CAS  PubMed  Google Scholar 

  • Varaljay, V.A., Robidart, J., Preston, C.M., Gifford, S.M., Durham, B.P., Burns, A.S., Ryan, J.P., Marin Roman, I., Kiene, R.P., Zehr, J.P., et al. (2015). Erratum: Single-taxon field measurements of bacterial gene regulation controlling DMSP fate. ISME J 9, 1692.

    Article  PubMed  PubMed Central  Google Scholar 

  • Veilleux, H.D., Misutka, M.D., and Glover, C.N. (2021). Environmental DNA and environmental RNA: current and prospective applications for biological monitoring. Sci Total Environ 782, 146891.

    Article  CAS  PubMed  Google Scholar 

  • Verdier, H., Konecny-Dupre, L., Marquette, C., Reveron, H., Tadier, S., Grémillard, L., Barthès, A., Datry, T., Bouchez, A., and Lefébure, T. (2022). Passive sampling of environmental DNA in aquatic environments using 3D-printed hydroxyapatite samplers. Mol Ecol Resour 22, 2158–2170.

    Article  CAS  PubMed  Google Scholar 

  • von Ammon, U., Pochon, X., Casanovas, P., Trochel, B., Zirngibl, M., Thomas, A., Witting, J., Joyce, P., and Zaiko, A. (2023). Net overboard: comparing marine eDNA sampling methodologies at sea to unravel marine biodiversity. Mol Ecol Resour 23, 440–452.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Liu, P., Chang, J., Li, C., Xie, F., and Jiang, J. (2021a). Development of an eDNA metabarcoding tool for surveying the world’s largest amphibian. Cur Zool 68, 608–614.

    Article  Google Scholar 

  • Wang, K., Shen, Y., Yang, Y., Gan, X., Liu, G., Hu, K., Li, Y., Gao, Z., Zhu, L., Yan, G., et al. (2019a). Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation. Nat Ecol Evol 3, 823–833.

    Article  PubMed  Google Scholar 

  • Wang, S., Yan, Z., Hänfling, B., Zheng, X., Wang, P., Fan, J., and Li, J. (2021b). Methodology of fish eDNA and its applications in ecology and environment. Sci Total Environ 755, 142622.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y., Gao, Z.M., Li, J., He, L.S., Cui, G.J., Li, W.L., Chen, J., Xin, Y.Z., Cai, D.S., and Zhang, A.Q. (2019b). Hadal water sampling by in situ microbial filtration and fixation (ISMIFF) apparatus. Deep Sea Res Part I Oceanogr Res Papers 144, 132–137.

    Article  Google Scholar 

  • Wang, Z., Huang, G., Huang, M., Dai, Q., Hu, Y., Zhou, J., and Wei, F. (2023). Global patterns of phylogenetic diversity and transmission of bat coronavirus. Sci China Life Sci 66, 861–874.

    Article  PubMed  Google Scholar 

  • Wei, J., Wang, M., Jiang, L., Yu, X., Mikelsons, K., and Shen, F. (2021). Global estimation of suspended particulate matter from satellite ocean color imagery. JGR Oceans 126, e2021JC017303.

    Article  PubMed  Google Scholar 

  • Wei, X.Y., Liu, L., Hu, H., Jia, H.J., Bu, L.K., and Pei, D.S. (2023). Ultra-sensitive detection of ecologically rare fish from eDNA samples based on the RPA-CRISPR/Cas12a technology. iScience 26, 107519.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei, Z.F., Li, W.L., Li, J., Chen, J., Xin, Y.Z., He, L.S., and Wang, Y. (2020). Multiple in situ Nucleic Acid Collections (MISNAC) from deep-sea waters. Front Mar Sci 7, 81.

    Article  Google Scholar 

  • West, K.M., Stat, M., Harvey, E.S., Skepper, C.L., DiBattista, J.D., Richards, Z.T., Travers, M.J., Newman, S.J., and Bunce, M. (2020). eDNA metabarcoding survey reveals fine-scale coral reef community variation across a remote, tropical island ecosystem. Mol Ecol 29, 1069–1086.

    Article  CAS  PubMed  Google Scholar 

  • Wilcox, T.M., McKelvey, K.S., Young, M.K., Jane, S.F., Lowe, W.H., Whiteley, A.R., and Schwartz, M.K. (2013). Robust detection of rare species using environmental DNA: the importance of primer specificity. PLoS ONE 8, e59520.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams, M., Hernandez, C., O’Sullivan, A.M., April, J., Regan, F., Bernatchez, L., and Parle-McDermott, A. (2021). Comparing CRISPR-Cas and qPCR eDNA assays for the detection of Atlantic salmon (Salmo salar L.). Environ DNA 3, 297–304.

    Article  CAS  Google Scholar 

  • Williams, M., O’Grady, J., Ball, B., Carlsson, J., de Eyto, E., McGinnity, P., Jennings, E., Regan, F., and Parle-McDermott, A. (2019). The application of CRISPR-Cas for single species identification from environmental DNA. Mol Ecol Resour 19, 1106–1114.

    Article  CAS  PubMed  Google Scholar 

  • Winslow, L.A., Dugan, H.A., Buelow, H.N., Cronin, K.D., Priscu, J.C., Takacs-Vesbach, C., and Doran, P.T. (2014). Autonomous year-round sampling and sensing to explore the physical and biological habitability of permanently ice-covered Antarctic Lakes. Mar Technol Soc J 48, 8–17.

    Article  Google Scholar 

  • Wood, S.A., Biessy, L., Latchford, J.L., Zaiko, A., von Ammon, U., Audrezet, F., Cristescu, M.E., and Pochon, X. (2020). Release and degradation of environmental DNA and RNA in a marine system. Sci Total Environ 704, 135314.

    Article  CAS  PubMed  Google Scholar 

  • Xiong, F., Shu, L., Zeng, H., Gan, X., He, S., and Peng, Z. (2022). Methodology for fish biodiversity monitoring with environmental DNA metabarcoding: The primers, databases and bioinformatic pipelines. Water Biol Secur 1, 100007.

    Article  Google Scholar 

  • Xu, B., Zhu, Y., Cao, C., Chen, H., Jin, Q., Li, G., Ma, J., Yang, S.L., Zhao, J., Zhu, J., et al. (2022). Recent advances in RNA structurome. Sci China Life Sci 65, 1285–1324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamahara, K.M., Demir-Hilton, E., Preston, C.M., Marin Iii, R., Pargett, D., Roman, B., Jensen, S., Birch, J.M., Boehm, A.B., and Scholin, C.A. (2015). Simultaneous monitoring of faecal indicators and harmful algae using an in-situ autonomous sensor. Lett Appl Microbiol 61, 130–138.

    Article  CAS  PubMed  Google Scholar 

  • Yamahara, K.M., Preston, C.M., Birch, J., Walz, K., Marin Iii, R., Jensen, S., Pargett, D., Roman, B., Ussler Iii, W., Zhang, Y., et al. (2019). In situ autonomous acquisition and preservation of marine environmental DNA using an autonomous underwater vehicle. Front Mar Sci 6, 373.

    Article  Google Scholar 

  • Yang, L., Sun, N., Zeng, H., Wang, Y., Chen, W., Ding, Z., Liu, Y., Wang, J., Meng, M., Shen, Y., et al. (2023). Enlarged fins of Tibetan catfish provide new evidence of adaptation to high plateau. Sci China Life Sci 66, 1554–1568.

    Article  CAS  PubMed  Google Scholar 

  • Yang, X., Liu, H., Ma, Z., Zou, Y., Zou, M., Mao, Y., Li, X., Wang, H., Chen, T., Wang, W., et al. (2019). Chromosome-level genome assembly of Triplophysa tibetana, a fish adapted to the harsh high-altitude environment of the Tibetan Plateau. Mol Ecol Resour 19, 1027–1036.

    Article  CAS  PubMed  Google Scholar 

  • Yao, M., Zhang, S., Lu, Q., Chen, X., Zhang, S.Y., Kong, Y., and Zhao, J. (2022). Fishing for fish environmental DNA: ecological applications, methodological considerations, surveying designs, and ways forward. Mol Ecol 31, 5132–5164.

    Article  PubMed  Google Scholar 

  • Yates, M.C., Derry, A.M., and Cristescu, M.E. (2021). Environmental RNA: a revolution in ecological resolution? Trends Ecol Evol 36, 601–609.

    Article  CAS  PubMed  Google Scholar 

  • Yoerger, D.R., Govindarajan, A.F., Howland, J.C., Llopiz, J.K., Wiebe, P.H., Curran, M., Fujii, J., Gomez-Ibanez, D., Katija, K., Robison, B.H., et al. (2021). A hybrid underwater robot for multidisciplinary investigation of the ocean twilight zone. Sci Robot 6, eabe1901.

    Article  PubMed  Google Scholar 

  • Yuan, M., Ding, R., Chen, S., and Duan, G. (2021). Advances in field detection based on CRISPR/Cas system. ACS Synth Biol 10, 2824–2832.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, C., and Zhang, B. (2023). RNA therapeutics: updates and future potential. Sci China Life Sci 66, 12–30.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y., Ryan, J.P., Hobson, B.W., Kieft, B., Romano, A., Barone, B., Preston, C.M., Roman, B., Raanan, B.Y., Pargett, D., et al. (2021). A system of coordinated autonomous robots for Lagrangian studies of microbes in the oceanic deep chlorophyll maximum. Sci Robot 6, eabb9138.

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

This work was supported by the National Natural Science Foundation of China (42330405, 32200367), and the National Key Research and Development Program of China (2022YFF0608200). This work was also supported by the National Natural Science Foundation of China (32325034, U2340216) and the Special Project for Social Development of Yunnan Province (202103AC100001) to Meng Yao. We thank Nathan Formel, Chengchi Fang and Liandong Yang for valuable suggestions of early drafts of this manuscript. We also thank the Scientific Data Center, Institute of Hydrobiology, CAS, and the Wuhan Branch, Supercomputing Center of CAS for their support.

Author information

Authors and Affiliations

  1. State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Suxiang Lu, Honghui Zeng, Fan Xiong & Shunping He

  2. Institute of Ecology, College of Urban and Environmental Sciences, Peking University, Beijing, 100871, China

    Meng Yao

  3. School of Life Sciences, Peking University, Beijing, 100871, China

    Meng Yao

  4. Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, China

    Shunping He

  5. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China

    Shunping He

Authors
  1. Suxiang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Honghui Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fan Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meng Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shunping He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Meng Yao or Shunping He.

Ethics declarations

The author(s) declare that they have no conflict of Interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, S., Zeng, H., Xiong, F. et al. Advances in environmental DNA monitoring: standardization, automation, and emerging technologies in aquatic ecosystems. Sci. China Life Sci. (2024). https://doi.org/10.1007/s11427-023-2493-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11427-023-2493-5

Search

Navigation