Can DNA-based ecosystem assessments quantify species abundance? Testing primer bias and biomass-sequence relationships with an innovative metabarcoding protocol

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Elbrecht, Vasco ^a   Leese, Florian ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE SUBUNIT I; PRIMER DNA; UNCLASSIFIED DRUG; DNA; FRESH WATER;

ANIMAL TISSUE; ARTICLE; BIOMASS; CONTROLLED STUDY; DIPTERA; DNA BARCODING; DNA DETERMINATION; DNA METABARCODING; DNA REPLICATION; EPHEMEROPTERA; FRESHWATER SPECIES; GENE LIBRARY; GENE SEQUENCE; GENETIC VARIABILITY; HAPLOTYPE; HIGH THROUGHPUT SEQUENCING; LARVA; LIMIT OF DETECTION; NONHUMAN; PLECOPTERA; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; POPULATION RECOVERY; REPRODUCIBILITY; SPECIES DIVERSITY; TAXONOMIC IDENTIFICATION; TRICHOPTERA; ANIMAL; BIODIVERSITY; CLASSIFICATION; ECOSYSTEM; GENETICS; ODONATA; PROCEDURES; SPECIES DIFFERENCE;

ANIMALS; BIODIVERSITY; BIOMASS; DIPTERA; DNA; DNA BARCODING, TAXONOMIC; DNA PRIMERS; ECOSYSTEM; ELECTRON TRANSPORT COMPLEX IV; FRESH WATER; HAPLOTYPES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; ODONATA; POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SPECIES SPECIFICITY;

EID: 84941286809     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130324     Document Type: Article

References (57)

1. Blaxter M. Molecular systematics: Counting angels with DNA. Nature. 2003:122-124. doi: 10.1038/421122a
2. Rockström J, Steffen W, Noone K, Persson A, Chapin FS, Lambin EF, et al. A safe operating space for humanity. Nature. 2009;461:472-475. doi: 10.1038/461472a PMID: 19779433
3. Millennium Ecosystem Assessment (2004) Ecosystems and Human Well-being: Synthesis. Island Press, Washington, D. C.
4. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, et al. Biodiversity loss and its impact on humanity. Nature. 2012;486:59-67. doi: 10.1038/nature11148 PMID: 22678280
5. Pfrender ME, Hawkins CP, Bagley M, Courtney GW, Creutzburg BR, Epler JH, et al. Assessing macroinvertebrate biodiversity in freshwater ecosystems: advances and challenges in DNA-based approaches. Q Rev Biol. 2010;85:319-340. PMID: 20919633
6. Vörösmarty CJ, McIntyre PB, Gessner MO, Dudgeon D, Prusevich A, Green P, et al. Global threats to human water security and river biodiversity. Nature. 2010;467:555-561. doi: 10.1038/nature09440 PMID: 20882010
7. Dudgeon D, Arthrington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, et al. Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev. 2005;81:163. doi: 10. 1017/S1464793105006950 PMID: 16336747
8. Meier C, Haase P, Rolauffs P, Schindehütte K, Schöll F, Sundermann A, et al. Methodisches Handbuch Fließgewässerbewertung. 2006;: 1-110.
9. Kenney MA, Sutton-Grier AE, Smith RF, Gresens SE. Benthic macroinvertebrates as indicators of water quality: The intersection of science and policy. Terr Arthropod Rev. 2009;2:99-128. doi: 10. 1163/187498209X12525675906077
10. Haase P, Pauls SU, Schindehütte K, Sundermann A. First audit of macroinvertebrate samples from an EU Water Framework Directive monitoring program: human error greatly lowers precision of assessment results. J North Am Benthol Soc. 2010;29:1279-1291. doi: 10.1899/09-183.1
11. Merritt RW, Berg MB, Cummins KW. An Introduction to the Aquatic Insects of North America. 2009.
12. Pauls SU, Graf W, Haase P, Lumbsch HT, Waringer J. Grazers, shredders and filtering carnivores-The evolution of feeding ecology in Drusinae (Trichoptera: Limnephilidae): Insights from a molecular phylogeny. Mol Phylogenet Evol. 2008;46:776-791. doi: 10.1016/j.ympev. 2007.11.003 PMID: 18171625
13. Jones FC. Taxonomic sufficiency: The influence of taxonomic resolution on freshwater bioassessments using benthic macroinvertebrates. Environ Rev. 2008;16:45-69. doi: 10.1139/A07-010
14. Stein ED, Martinez MC, Stiles S, Miller PE, Zakharov EV. Is DNA Barcoding Actually Cheaper and Faster than Traditional Morphological Methods: Results from a Survey of Freshwater Bioassessment Efforts in the United States? Casiraghi M, editor. PLoS ONE. 2014;9:e95525. doi: 10.1371/journal. pone.0095525.t005 PMID: 24755838
15. Hebert PDN, Ratnasingham S, De Waard JR. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Biol Sci. 2003;270:S96-S99. doi: 10. 1098/rsbl.2003.0025
16. Zhou X, Adamowicz SJ, Jacobus LM, De Walt RE, Hebert PD. Towards a comprehensive barcode library for arctic life-Ephemeroptera, Plecoptera, and Trichoptera of Churchill, Manitoba, Canada. Front Zool. 2009;6:30. doi: 10.1186/1742-9994-6-30 PMID: 20003245
17. Zhou X, Jacobus LM, De Walt RE, Adamowicz SJ, Hebert PDN. Ephemeroptera, Plecoptera, and Trichoptera fauna of Churchill (Manitoba, Canada): insights into biodiversity patterns from DNA barcoding. J North Am Benthol Soc. 2010;29:814-837. doi: 10.1899/09-121.1
18. Sweeney BW, Battle JM, Jackson JK, Dapkey T. Can DNA barcodes of stream macroinvertebrates improve descriptions of community structure and water quality? J North Am Benthol Soc. 2011;30:195-216. doi: 10.1899/10-016.1
19. Hebert PDN, Cywinska A, Ball SL, De Waard JR. Biological identifications through DNA barcodes. Proc R Soc Lond B Biol Sci. The Royal Society; 2003;270:313-321. doi: 10.1098/rspb.2002.2218
20. Zhou X, Kjer KM, Morse JC. Associating larvae and adults of Chinese Hydropsychidae caddisflies (Insecta: Trichoptera) using DNA sequences. J North Am Benthol Soc. 2007;26:719-742. doi: 10. 1899/06-089.1
21. Ekrem T, Stur E, Hebert PDN. Females do count: Documenting Chironomidae (Diptera) species diversity using DNA barcoding. Org Divers Evol. 2010;10:397-408. doi: 10.1007/s13127-010-0034-y
22. Ratnasingham S, Hebert P. BOLD: The Barcode of Life Data System (http://www.barcodinglife.org). Mol Ecol Notes. 2007;7:355-364. doi: 10.1111/j.1471-8286.2006.01678.x PMID: 18784790
23. Hopkins GW, Freckleton RP. Declines in the numbers of amateur and professional taxonomists: implications for conservation. Anim Conserv. 2002;5:245-249. doi: 10.1017/S1367943002002299
24. Agnarsson I, Kuntner M. Taxonomy in a changing world: seeking solutions for a science in crisis. Syst Biol. 2007;56:531-539. doi: 10.1080/10635150701424546 PMID: 17562477
25. Jackson JK, Battle JM, White BP, Pilgrim EM. Cryptic biodiversity in streams: a comparison of macroinvertebrate communities based on morphological and DNA barcode identifications. Freshw Sci. 2014;33:312-324. doi: 10.1086/675225 PMID: 24309212
26. Mächler E, Deiner K, Steinmann P, Altermatt F. Utility of environmental DNA for monitoring rare and indicator macroinvertebrate species. Freshw Sci. 2014. doi: 10.1086/678128
27. Taberlet P, Coissac E, Hajibabaei M, Rieseberg LH. Environmental DNA. Mol Ecol. 2012;21:1789-1793. doi: 10.1111/j.1365-294X.2012.05542.x PMID: 22486819
28. Bohmann K, Evans A, Gilbert MTP, Carvalho GR, Creer S, Knapp M, et al. Environmental DNA for wildlife biology and biodiversity monitoring. Trends Ecol Evol (Amst). 2014;29:358-367. doi: 10.1016/j. tree.2014.04.003 PMID: 24821515
29. Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P. Who is eating what: diet assessment using next generation sequencing. Mol Ecol. 2012;21:1931-1950. doi: 10.1111/j. 1365-294X.2011.05403.x PMID: 22171763
30. Poisot T, Péquin B, Gravel D. High-Throughput Sequencing: A roadmap toward Community ecology. Ecol Evol. 2013;3:1125-1139. doi: 10.1002/ece3.508 PMID: 23610649
31. Yu DW, Ji Y, Emerson BC, Wang X, Ye C, Yang C, et al. Biodiversity soup: metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods Ecol Evol. 2012;3:613-623. doi: 10.1111/j.2041-210X.2012.00198.x
32. Gibson J, Shokralla S, Porter TM, King I, Van Konynenburg S, Janzen DH, et al. Simultaneous assessment of the macrobiome and microbiome in a bulk sample of tropical arthropods through DNA metasystematics. Proc Natl Acad Sci. 2014;111:8007-8012. doi: 10.1073/pnas.1406468111 PMID: 24808136
33. Zimmermann J, Glöckner G, Jahn R, Enke N, Gemeinholzer B. Metabarcoding vs. morphological identification to assess diatom diversity in environmental studies. Mol Ecol Resour. 2014;1-17. doi: 10. 1111/1755-0998.12336
34. Hajibabaei M, Shokralla S, Zhou X, Singer G, Baird DJ. Environmental barcoding: A next-generation sequencing approach for biomonitoring applications using river benthos. PLoS ONE. 2011;6:e17497. doi: 10.1371/journal.pone.0017497 PMID: 21533287
35. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: Open-Source, Platform-Independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537-7541. doi: 10.1128/AEM.01541-09 PMID: 19801464
36. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-336. doi: 10. 1038/nmeth0510-335 PMID: 20383131
37. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996-998. doi: 10.1038/nmeth.2604 PMID: 23955772
38. Carew ME, Pettigrove VJ, Metzeling L, Hoffmann AA. Environmental monitoring using next generation sequencing: rapid identification of macroinvertebrate bioindicator species. Front Zool. 2013;10:1-1. doi: 10.1186/1742-9994-10-45 PMID: 23356547
39. Piñol J, Mir G, Gomez-Polo P, Agustí N. Universal and blocking primer mismatches limit the use of high-throughput DNA sequencing for the quantitative metabarcoding of arthropods. Mol Ecol Resour. 2014;1-12. doi: 10.1111/1755-0998.12355
40. Krueger F, Andrews SR, Osborne CS. Large scale loss of data in low-diversity Illumina sequencing libraries can be recovered by deferred cluster calling. Preiss T, editor. PLoS ONE. 2011;6:e16607. doi: 10.1371/journal.pone.0016607.s002 PMID: 21305042
41. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Marine Biol Biotechnol. 1994;3:294-299. PMID: 7881515
42. Lundberg DS, Yourstone S, Mieczkowski P, Jones CD, Dangl JL. Practical innovations for highthroughput amplicon sequencing. Nat Methods. 2013;10:999-1002. doi: 10.1038/nmeth.2634 PMID: 23995388
43. Elbrecht V, Feld CK, Gies M, Hering D, Sondermann M. Genetic diversity and dispersal potential of the stonefly Dinocras cephalotes in a central European low mountain range. Freshw Sci. 2014;33:181-192. doi: 10.1086/674536 PMID: 25000790
44. Sunnucks P, Hales DF. Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol. 1996;13:510-524. PMID: 8742640
45. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet journal. 2011;17:10-12.
46. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. doi: 10.1186/1471-2105-10-421 PMID: 20003500
47. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. 2014.
48. Elbrecht V, Poettker L, John U, Leese F. The complete mitochondrial genome of the stonefly Dinocras cephalotes (Plecoptera, Perlidae). Mitochondrial DNA. 2013. doi: 10.3109/19401736.2013.830301
49. Polz MF, Cavanaugh CM. Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microbiol. 1998;64:3724-3730. PMID: 9758791
50. Zhou X, Li Y, Liu S, Yang Q, Su X, Zhou L, et al. Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. Gigascience. 2013;2:4. doi: 10. 1186/2047-217X-2-4 PMID: 23587339
51. Ranasinghe JA, Stein ED, Miller PE, Weisberg SB. Performance of Two Southern California Benthic Community Condition Indices Using Species Abundance and Presence-Only Data: Relevance to DNA Barcoding. Crandall KA, editor. PLoS ONE. 2012;7:e40875. doi: 10.1371/journal.pone.0040875 PMID: 22879881
52. Aylagas E, Borja A, Rodríguez-Ezpeleta N. Environmental status assessment using DNA metabarcoding: towards a genetics based Marine Biotic Index (gAMBI). Consuegra S, editor. PLoS ONE. 2014;9:e90529. doi: 10.1371/journal.pone.0090529 PMID: 24603433
53. Meusnier I, Singer GA, Landry J-F, Hickey DA, Hebert PD, Hajibabaei M. A universal DNA mini-barcode for biodiversity analysis. BMC Genomics. 2008;9:214. doi: 10.1186/1471-2164-9-214 PMID: 18474098
54. Deagle BE, Jarman SN, Coissac E, Pompanon F, Taberlet P. DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match. Biol Lett. 2014;10:20140562-20140562. doi: 10.1098/rsbl.2014.0562 PMID: 25209199
55. Clarke LJ, Soubrier J, Weyrich LS, Cooper A. Environmental metabarcodes for insects: in silicoPCR reveals potential for taxonomic bias. Mol Ecol Resour. 2014;14:1160-1170. doi: 10.1111/1755-0998. 12265 PMID: 24751203
56. Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E. Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol. 2012;21:2045-2050. doi: 10.1111/j.1365-294X. 2012.05470.x PMID: 22486824
57. Ji Y, Ashton L, Pedley SM, Edwards DP, Tang Y, Nakamura A, et al. Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding. Holyoak M, editor. Ecol Lett. 2013;16:1245-1257. doi: 10.1111/ele.12162 PMID: 23910579