Environmental conditions influence eDNA persistence in aquatic systems

Environmental Science and Technology

Volumn 48, Issue 3, 2014, Pages 1819-1827

  Barnes, Matthew A ^a   Turner, Cameron R ^a   Jerde, Christopher L ^a   Renshaw, Mark A ^a   Chadderton, W Lindsay ^b   Lodge, David M ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b THE NATURE CONSERVANCY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; FRESH WATER;

ANIMAL; CARP; CHEMISTRY; ENVIRONMENT; POLYMERASE CHAIN REACTION;

ANIMALS; CARPS; DNA; ENVIRONMENT; FRESH WATER; POLYMERASE CHAIN REACTION;

EID: 84893602243     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es404734p     Document Type: Article

References (92)

1. Beja-Pereira, A.; Oliveira, R.; Schwartz, M. K.; Luikart, G. Advancing ecological understanding through technological transformation in noninvasive genetics Mol. Ecol. Resour. 2009, 9, 1279-1301
2. Taberlet, P.; Coissac, E.; Hajibabaei, M.; Rieseberg, L. H. Environmental DNA Mol. Ecol. 2012, 21, 1789-1793
3. Ficetola, G. F.; Miaud, C.; Pompanon, F.; Taberlet, P. Species detection using environmental DNA from water samples Biol. Lett. 2008, 4, 423-425
4. Dejean, T.; Valentini, A.; Miquel, C.; Taberlet, P.; Bellemain, E.; Miaud, C. Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus J. Appl. Ecol. 2012, 49, 953-959
5. Goldberg, C. S.; Pilliod, D. S.; Arkle, R. S.; Waits, L. P. Molecular detection of vertebrates in stream water: a demonstration using rocky mountain tailed frogs and Idaho giant salamanders PLoS One 2011, 6, e22746
6. Pilliod, D. S.; Goldberg, C. S.; Arkle, R. S.; Waits, L. P. Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples Can. J. Fish. Aquat. Sci. 2013, 70, 1123-1130
7. Jerde, C. L.; Mahon, A. R.; Chadderton, W. L.; Lodge, D. M. "Sight-unseen" detection of rare aquatic species using environmental DNA Conserv. Lett. 2011, 4, 150-157
8. Thomsen, P. F.; Kielgast, J.; Iversen, L. L.; Wiuf, C.; Rasmussen, M.; Gilbert, M. T. P.; Orlando, L.; Willerslev, E. Monitoring endangered freshwater biodiversity using environmental DNA Mol. Ecol. 2012, 21, 2565-2573
9. Takahara, T.; Minamoto, T.; Yamanaka, H.; Doi, H.; Kawabata, Z. Estimation of fish biomass using environmental DNA PLoS One 2012, 7, e35868
10. Takahara, T.; Minamoto, T.; Doi, H. Using environmental DNA to estimate the distribution of an invasive fish species in ponds PLoS ONE 2013, 8, e56584
11. Thomsen, P. F.; Kielgast, J.; Iversen, L. L.; Møller, P. R.; Rasmussen, M.; Willerslev, E. Detection of a diverse marine fish fauna using environmental DNA from seawater samples PLoS One 2012, 7, e41732
12. Foote, A. D.; Thomsen, P. F.; Sveegaard, S.; Wahlberg, M.; Kielgast, J.; Kyhn, L. A.; Salling, A. B.; Galatius, A.; Orlando, L.; Gilbert, M. T. P. Investigating the potential use of environmental DNA (eDNA) for genetic monitoring of marine mammals PLoS One 2012, 7, e41781
13. Sutherland, W. J.; Bardsley, S.; Clout, M.; Depledge, M. H.; Dicks, L. V.; Fellman, L.; Fleishman, E.; Gibbons, D. W.; Keim, B.; Lickorish, F.; Margerison, C.; Monk, K. A.; Norris, K.; Peck, L. S.; Prior, S. V.; Scharlemann, J. P. W.; Spalding, M. D.; Watkinson, A. R. A horizon scan of global conservation issues for 2013 Trends Ecol. Evol. 2013, 28, 16-22
14. Dejean, T.; Valentini, A.; Duparc, A.; Pellier-Cuit, S.; Pompanon, F.; Taberlet, P.; Miaud, C. Persistence of environmental DNA in freshwater ecosystems PLoS One 2011, 6, e23398
15. Goldberg, C. S.; Sepulveda, A.; Ray, A.; Baumgardt, J.; Waits, L. P. Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum) Freshwater Sci. 2013, 32, 792-800
16. Schwartz, M. K.; Luikart, G.; Waples, R. S. Genetic monitoring as a promising tool for conservation and management Trends Ecol. Evol. 2007, 22, 25-33
17. Lodge, D. M.; Turner, C. R.; Jerde, C. L.; Barnes, M. A.; Chadderton, L.; Egan, S. P.; Feder, J. L.; Mahon, A. R.; Pfrender, M. E. Conservation in a cup of water: estimating biodiversity and population abundance from environmental DNA Mol. Ecol. 2012, 21, 2555-2558
18. Dodds, W. K. Freshwater Ecology Concepts and Environmental Applications; Academic Press: San Diego, CA, 2002.
19. Carpenter, S. R.; Kitchell, J. F.; Hodgson, J. R. Cascading trophic interactions and lake productivity BioScience 1985, 35, 634-639
20. McIntyre, P. B.; Flecker, A. S.; Vanni, M. J.; Hood, J. M.; Taylor, B. W.; Thomas, S. A. Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots? Ecology 2008, 89, 2335-2346
21. Gulis, V.; Suberkropp, K. Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream Freshwater Biol. 2003, 48, 123-134
22. American Public Health Association. Standard Methods for the Examination of Water and Wastewater; Port City Press: Baltimore, MD, 1999.
23. Delzer, G. C.; McKenzie, S. W. Five-day biochemical oxygen demand; U.S. Geological Survey Techniques of Water-Resources Investigations, 3 rd ed., 2003; Book 9, Chapter A7, Section 7.0; http://pubs.water.usgs.gov/twri9A/.
24. Coyne, K. J.; Hutchins, D. A.; Hare, C. E.; Cary, S. C. Assessing temporal and spatial variability in Pfiesteria piscicida distributions using molecular probing techniques Aquat. Microb. Ecol. 2001, 24, 275-285
25. Ririe, K. M.; Rasmussen, R. P.; Wittwer, C. T. Product differentiation by analysis of DNA melting curves during the polymerase chain reaction Anal. Biochem. 1997, 245, 154-160
26. Betancourt, W. Q.; Fujioka, R. S. Bacteroides spp. as reliable marker of sewage contamination in Hawaii's environmental waters using molecular techniques Water Sci. Technol. 2006, 54, 101-107
27. Morrison, T. B.; Weis, J. J.; Wittwer, C. T. Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification BioTechniques 1998, 24, 954-962
28. Ellison, S. L. R.; English, C. A.; Burns, M. J.; Keer, J. T. Routes to improving the reliability of low level DNA analysis using real-time PCR BMC Biotechnol. 2006, 6, 33
29. Robin, X.; Turck, N.; Hainard, A.; Tiberti, N.; Lisacek, F.; Sanchez, J.; Müller, M. pROC: an open-source package for R and S+ to analyze and compare ROC curves BMC Bioinf. 2011, 12, 77
30. Hosmer, D. W.; Lemeshow, S. Applied Logistic Regression, 2 nd ed.; Wiley Inter-Science: New York, NY, 2000.
31. Siuda, W.; Chróst, R. Concentration and susceptibility of dissolved DNA for enzyme degradation in lake water-some methodological remarks Aquat. Microb. Ecol. 2000, 21, 195-201
32. DeFlaun, M. F.; Paul, J. H. Detection of exogenous gene sequences in dissolved DNA from aquatic environments Microb. Ecol. 1989, 18, 21-28
33. Dell'Anno, A.; Bompadre, S.; Danovaro, R. Quantification, base composition, and fate of extracellular DNA in marine sediments Limnol. Oceanogr. 2002, 47, 899-905
34. Pietramellara, G.; Ceccherini, M. T.; Ascher, J.; Nannipieri, P. Persistence of transgenic and not transgenic extracellular DNA in soil and bacterial transformation Riv. Biol.-Biol. Forum 2006, 99, 37-68
35. Singh, A.; Billingsley, K.; Ward, O. Composting: a potentially safe process for disposal of genetically modified organisms Crit. Rev. Biotechnol. 2006, 26, 1-16
36. Levy-Booth, D. J.; Campbell, R. G.; Gulden, R. H.; Hart, M. M.; Powell, J. R.; Klironomos, J. N.; Pauls, K. P.; Swanton, C. J.; Trevors, J. T.; Dunfield, K. E. Cycling of extracellular DNA in the soil environment Soil Biol. Biochem. 2007, 39, 2977-2991
37. Nielsen, K. M.; Johnsen, P. J.; Bensasson, D.; Daffonchio, D. Release and persistence of extracellular DNA in the environment Environ. Biosaf. Res. 2007, 6, 37-53
38. Pietramellara, G.; Ascher, J.; Borgogni, F.; Ceccherini, M. T.; Guerri, G.; Nannipieri, P. Extracellular DNA in soil and sediment: fate and ecological relevance Biol. Fertil. Soils 2009, 45, 219-235
39. Romanowski, G.; Lorenz, M. G.; Wackernagel, W. Plasmid DNA in a groundwater aquifer microcosm-adsorption, DNAase resistance and natural genetic transformation of Bacillus subtilis Mol. Ecol. 1993, 2, 171-181
40. Ogram, A. V.; Mathot, M. L.; Harsh, J. B.; Boyle, J.; Pettigrew, C. A., Jr. Effects of DNA polymer length on its adsorption to soils Appl. Environ. Microbiol. 1994, 60, 393-396
41. Gallori, E.; Bazzicalupo, M.; Dal Canto, L.; Fani, R.; Nannipieri, P.; Vettori, C.; Stotzky, G. Transformation of Bacillus subtilis by DNA bound on clay in non-sterile soil FEMS Microbiol. Ecol. 1994, 15, 119-126
42. Poly, F.; Chenu, C.; Simonet, P.; Rouiller, J.; Monrozier, L. J. Differences between linear chromosomal and supercoiled plasmid DNA in their mechanisms and extent of adsorption on clay minerals Langmuir 2000, 1233-1238
43. Lenon, J. T. Diversity and metabolism of marine bacteria cultivated on dissolved DNA Appl. Environ. Microbiol. 2007, 73, 2799-2805
44. Lindahl, T. Instability and decay of the primary structure of DNA Nature 1993, 362, 709-715
45. Ceccherini, M.; Poté, J.; Kay, E.; Van, V. T.; Pietramellara, G.; Nannipieri, P.; Vogel, T. M.; Simonet, P. Degradation and transformability of DNA from transgenic leaves Appl. Environ. Microbiol. 2003, 69, 673-678
46. Bravo, A. G.; Wildi, W.; Poté, J. Kinetics of plant material mass loss and DNA release in freshwater column Ecotoxicol. Environ. Saf. 2010, 73, 1548-1552
47. Widmer, F.; Seidler, R. J.; Watrud, L. S. Sensitive detection of transgenic plant marker gene persistence in soil microcosms Mol. Ecol. 1996, 5, 603-613
48. Widmer, F.; Seidler, R. J.; Donegan, K. K.; Reed, G. L. Quantification of transgenic plant marker gene persistence in the field Mol. Ecol. 1997, 6, 1-7
49. Poté, J.; Rossé, P.; Rosselli, W.; Van, V. T.; Wildi, W. Kinetics of mass and DNA decomposition in tomato leaves Chemosphere 2005, 61, 677-684
50. Walters, S. P.; Yamahara, K. M.; Boehm, A. B. Persistence of nucleic acid markers of health-relevant organisms in seawater microcosms: implications for their use in assessing risk in recreational waters Water Res. 2009, 43, 4929-4939
51. Boere, A. C.; Damsté, J. S. S.; Rijpstra, W. I. C.; Volkman, J. K.; Coolen, M. J. L. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation Org. Geochem. 2011, 42, 1216-1225
52. Kreader, C. A. Persistence of PCR-detectable Bacteroides distasonis from human feces in river water Appl. Environ. Microbiol. 1998, 64, 4103-4105
53. Hofreiter, M.; Serre, D.; Poinar, H. N.; Kuch, M.; Pääbo, S. Ancient DNA Nat. Rev. Genet. 2001, 2, 353-359
54. Okabe, S.; Shimazu, Y. Persistence of host-specific Bacteroides- Prevotella 16S rRNA genetic markers in environmental waters: effects of temperature and salinity Appl. Microbiol. Biotechnol. 2007, 76, 935-944
55. Corinaldesi, C.; Beolchini, F.; Dell'Anno, A. Damage and degradation rates of extracellular DNA in marine sediments: implications for the preservation of gene sequences Mol. Ecol. 2008, 17, 3939-3951
56. Poté, J.; Ackermann, R.; Wildi, W. Plant leaf mass loss and DNA release in freshwater sediments Ecotoxicol. Environ. Saf. 2009, 72, 1378-1383
57. Dick, L. K.; Stelzer, E. A.; Bertke, E. E.; Fong, D. L.; Stoeckel, D. M. Relative decay of Bacteroidales microbial source tracking markers and cultivated Escherichia coli in freshwater microcosms Appl. Environ. Microbiol. 2010, 76, 3255-3262
58. Fu, X. H.; Wang, L.; Le, Y. Q.; Hu, J. J. Persistence and renaturation efficiency of thermally treated waste recombinant DNA in defined aquatic microcosms J. Environ. Sci. Health, Part A: Toxic/Hazard. Subst. Environ. Eng. 2012, 47, 1975-1983
59. Borin, S.; Crotti, E.; Mapelli, F.; Tamagnini, I.; Corselli, C.; Daffonchio, D. DNA is preserved and maintains transforming potential after contact with brines of the deep anoxic hypersaline lakes of the Eastern Mediterranean Sea Saline Syst. 2008, 4, 10
60. Ravanat, J.; Douki, T.; Cadet, J. Direct and indirect effects of UV radiation on DNA and its components J. Photochem. Photobiol., B 2001, 63, 88-102
61. Bae, S.; Wuertz, S. Rapid decay of host-specific fecal Bacteroidales cells in seawater as measured by quantitative PCR with propidium monoazide Water Res. 2009, 43, 4850-4859
62. Bae, S.; Wuertz, S. Survival of host-associated bacteroidales cells and their relationship with Enterococcus spp., Campylobacter jejuni, Salmonella enterica serovar Typhimurium, and adenovirus in freshwater microcosms as measured by propidium monoazide-quantitative PCR Appl. Environ. Microbiol. 2012, 78, 922-32
63. Green, H. C.; Shanks, O. C.; Sivaganesan, M.; Haugland, R. A.; Field, K. G. Differential decay of human faecal Bacteroides in marine and freshwater Environ. Microbiol. 2011, 13, 3235-3249
64. Lorenz, M. G.; Wackernagel, W. Adsorption of DNA to sand and variable degradation rates of adsorbed DNA Appl. Environ. Microbiol. 1987, 53, 2948-52
65. Romanowski, G.; Lorenz, M. G.; Wackernagel, W. Adsorption of plasmid DNA to mineral surfaces and protection against DNase I Appl. Environ. Microbiol. 1991, 57, 1057-1061
66. Recorbet, G.; Picard, C.; Normand, P.; Simonet, P. Kinetics of the persistence of chromosomal DNA from genetically engineered Escherichia coli introduced into soil Appl. Environ. Microbiol. 1993, 59, 4289-4294
67. Blum, S. A. E.; Lorenz, M. G.; Wackernagel, W. Mechanism of retarded DNA degradation and prokaryotic origin of DNases in nonsterile soils Syst. Appl. Microbiol. 1997, 20, 513-521
68. Demanèche, S.; Jocteur-Monrozier, L.; Quiquampoix, H.; Simonet, P. Evaluation of biological and physical protection against nuclease degradation of clay-bound plasmid DNA Appl. Environ. Microbiol. 2001, 67, 293-299
69. Cai, P.; Huang, Q.; Zhang, X.; Chen, H. Binding and transformation of extracellular DNA in soil Pedosphere 2005, 15, 16-23
70. Douville, M.; Gagne, F.; Blaise, C.; Andre, C. Occurrence and persistence of Bacillus thuringiensis (Bt) and transgenic Bt corn cry1Ab gene from an aquatic environment Ecotoxicol. Environ. Saf. 2007, 66, 195-203
71. Cai, P.; Huang, Q.; Li, M.; Liang, W. Binding and degradation of DNA on montmorillonite coated by hydroxyl aluminum species Colloids Surf., B 2008, 62, 299-306
72. Romanowski, G.; Lorenz, M. G.; Sayler, G.; Wackernagel, W. Persistence of free plasmid DNA in soil monitored by various methods, including a transformation assay Appl. Environ. Microbiol. 1992, 58, 3012-3019
73. Cai, P.; Huang, Q.; Zhang, X.; Chen, H. Adsorption of DNA on clay minerals and various colloidal particles from an Alfisol Soil Biol. Biochem. 2006, 38, 471-476
74. Cai, P.; Huang, Q.; Zhang, X. Interactions of DNA with clay minerals and soil colloidal particles and protection against degradation by DNase Environ. Sci. Technol. 2006, 40, 2971-2976
75. Cai, P.; Huang, Q.; Chen, W.; Zhang, D.; Wang, K.; Jiang, D.; Liang, W. Soil colloids-bound plasmid DNA: effect on transformation of E. coli and resistance to DNase I degradation Soil Biol. Biochem. 2007, 39, 1007-1013
76. Saeki, K.; Kunito, T.; Sakai, M. Effect of Tris-HCl buffer on DNA adsorption by a variety of soil constituents Microbes Environ. 2011, 26, 88-91
77. DeFlaun, M. F.; Paul, J. H.; Davis, D. Simplified method for dissolved DNA determination in aquatic environments Appl. Environ. Microbiol. 1986, 52, 654-659
78. Alvarez, A. J.; Yumet, G. M.; Santiago, C. L.; Toranzos, G. A. Stability of manipulated plasmid DNA in aquatic environments Environ. Toxicol. Water Qual. 1996, 11, 129-135
79. England, L. S.; Lee, H.; Trevors, J. T. Persistence of Pseudomonas aureofaciens strains and DNA in soil Soil Biol. Biochem. 1997, 29, 1521-1527
80. Kim, C.; Kwak, M.; Lee, S. Structural and functional stability of the genetic recombinant plasmid pCUI03 in different water environments J. Microbiol. 1996, 34, 241-247
81. Matsui, K.; Honjo, M.; Kawabata, Z. Estimation of the fate of dissolved DNA in thermally stratified lake water from the stability of exogenous plasmid DNA Aquat. Microb. Ecol. 2001, 26, 95-102
82. Paul, J. H.; Jeffrey, W. H.; DeFlaun, M. F. Dynamics of extracellular DNA in the marine environment Appl. Environ. Microbiol. 1987, 53, 170-179
83. Paul, J. H.; Jeffrey, W. H.; David, A. W.; DeFlaun, M. F.; Cazares, L. H. Turnover of extracellular DNA in eutrophic and oligotrophic freshwater environments of southwest Florida Appl. Environ. Microbiol. 1989, 55, 1823-1828
84. Zhu, B. Degradation of plasmid and plant DNA in water microcosms monitored by natural transformation and real-time polymerase chain reaction (PCR) Water Res. 2006, 40, 3231-3238
85. Dell'Anno, A.; Corinaldesi, C. Degradation and turnover of extracellular DNA in marine sediments: ecological and methodological considerations Appl. Environ. Microbiol. 2004, 70, 4384-4386
86. Mann, E. E.; Rice, K. C.; Boles, B. R.; Endres, J. L.; Ranjit, D.; Chandramohan, L.; Tsang, L. H.; Smeltzer, M. S.; Horswill, A. R.; Bayles, K. W. Modulation of eDNA release and degradation affects Staphylococcus aureus biofilm maturation PLoS One 2009, 4, e5822
87. Flemming, H.; Wingender, J. The biofilm matrix Nat. Rev. Microbiol. 2010, 8, 623-633
88. Corinaldesi, C.; Barucca, M.; Luna, G. M.; Dell'anno, A. Preservation, origin and genetic imprint of extracellular DNA in permanently anoxic deep-sea sediments Mol. Ecol. 2011, 20, 642-54
89. Schoenberg, S. A.; Benner, R.; Armstrong, A.; Sobecky, P.; Hodson, R. E. Effects of acid stress on aerobic decomposition of algal and aquatic macrophyte detritus: direct comparison in a radiocarbon assay Appl. Environ. Microbiol. 1990, 56, 237-244
90. Chamier, A. C. Effect of pH on microbial degradation of leaf litter in seven streams of the English Lake District Oecolgia 1987, 71, 491-500
91. Collier, K. J.; Chadderton, W. L.; Winterbourn, M. J. Breakdown and invertebrate colonisation of kamahi leaves in southern New Zealand streams New Zeal. Nat. Sci. 2006, 31, 137-149
92. Andersen, K.; Bird, K. L.; Rasmussen, M.; Haile, J.; Breuning-Madsen, H.; Kjaer, K. H.; Orlando, L.; Gilbert, M. T. P.; Willerslev, E. Meta-barcoding of "dirt" DNA from soil reflects vertebrate biodiversity Mol. Ecol. 2012, 21, 1966-1979