Environmental monitoring through protist next-generation sequencing metabarcoding: Assessing the impact of fish farming on benthic foraminifera communities

Molecular Ecology Resources

Volumn 14, Issue 6, 2014, Pages 1129-1140

  Pawlowski, Jan ^a   Esling, Philippe ^a,b   Lejzerowicz, Franck ^a   Cedhagen, Tomas ^c   Wilding, Thomas A ^d  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b IRCAM   (France)

^c AARHUS UNIVERSITY   (Denmark)

^d SCOTTISH MARINE INSTITUTE   (United Kingdom)

Author keywords

Bioinformatics phyloinformatics; DNA barcoding; Ecotoxicology; Environmental DNA; Protists

Indexed keywords

ANIMAL; BIODIVERSITY; CLASSIFICATION; DNA BARCODING; ENVIRONMENTAL MONITORING; EVALUATION STUDY; FISHERY; FORAMINIFER; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; HUMAN; PARASITOLOGY; PROCEDURES; SALMON; SEDIMENT; UNITED KINGDOM;

ANIMALS; BIODIVERSITY; DNA BARCODING, TAXONOMIC; ENVIRONMENTAL MONITORING; FISHERIES; FORAMINIFERA; GEOLOGIC SEDIMENTS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; SALMON; SCOTLAND;

EID: 84907953277     PISSN: 1755098X     EISSN: 17550998     Source Type: Journal    
DOI: 10.1111/1755-0998.12261     Document Type: Article

References (64)

1. Altin-Ballero DZ, Habura A, Goldstein ST (2013) Psammophaga sapela n.sp., a new monthalmous foraminiferan from coastal Georgia, USA: fine structure, gametogenesis, and phylogenetic placement. Journal of Foraminiferal Research, 43, 113-126.
2. Alve E (1995) Benthic foraminiferal responses to estuarine pollution-a review. Journal of Foraminiferal Research, 25, 190-203.
3. Angel DL, Verghese S, Lee JJ et al. (2000) Impact of a net cage fish farm on the distribution of benthic foraminifera in the northern Gulf of Eliat (Aqaba, Red Sea). Journal of Foraminiferal Research, 30, 54-65.
4. Baird DJ, Hajibabaei M (2012) Biomonitoring 2.0: a new paradigm in ecosystem assessment made possible by next-generation DNA sequencing. Molecular Ecology, 21, 2039-2044.
5. Bergin F, Kucuksezgin F, Uluturhan E et al. (2006) The response of benthic foraminifera and ostracoda to heavy metal pollution in Gulf of Izmir (Eastern Aegean Sea). Estuarine Coastal and Shelf Science, 66, 368-386.
6. Bik HM, Halanych KM, Sharma J, Thomas WK (2012) Dramatic Shifts in Benthic Microbial Eukaryote Communities following the Deepwater Horizon Oil Spill. PLoS One, 7, e38550.
7. Black KD (1998) The environmental interactions associated with fish culture. In: Biology of Farmed Fish (eds Black KD, Pickering AD), pp. 284-326. Sheffield Academic Press, Sheffield.
8. Borja A, Rodriguez JG, Black K et al. (2009) Assessing the suitability of a range of benthic indices in the evaluation of environmental impact of fin and shellfish aquaculture located in sites across Europe. Aquaculture, 293, 231-240.
9. Burridge L, Weis JS, Cabello F, Pizarro J, Bostick K (2010) Chemical use in salmon aquaculture: a review of current practices and possible environmental effects. Aquaculture, 306, 7-23.
10. Campbell B, Pauly D (2013) Mariculture: a global analysis of production trends since 1950. Marine Policy, 39, 94-100.
11. Carew ME, Pettigrove VJ, Metzeling L, Hoffmann AA (2013) Environmental monitoring using next generation sequencing: rapid identification of macroinvertebrate bioindicators species. Frontiers in Zoology, 10, 45.
12. Carroll ML, Cochrane S, Fieler R, Velvin R, White P (2003) Organic enrichment of sediments from salmon farming in Norway: an environmental factors, management practices and monitoring techniques. Aquaculture, 226, 165-180.
13. Cedhagen T (2006) Foraminifera in the Northeast Atlantic and Arctic Oceans, internal report. Aarhus University, 331 pp.
14. Chariton AA, Court LN, Hartley DM et al. (2010) Ecological assessment of estuarine sediments by pyrosequencing eukaryotic ribosomal DNA. Frontiers in Ecology and the Environment, 8, 233-238.
15. Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18, 117-143.
16. Clarke KR (1999) Nonmetric multivariate analysis in community-level ecotoxicology. Environmental Toxicology and Chemistry, 18, 118-127.
17. Corinaldesi C, Barucca M, Luna GM, Dell'Anno A (2011) Preservation, origin and genetic imprint of extracellular DNA in permanently anoxic deep-sea sediments. Molecular Ecology, 20, 642-654.
18. Craib JS (1965) A sampler for taking short undisturbed marine cores. ICES Journal of Marine Science, 30, 34-39.
19. Creer S, Fonseca VG, Porazinska DL et al. (2010) Ultrasequencing of the meiofaunal biosphere: practice, pitfalls and promises. Molecular Ecology, 19, 4-20.
20. Dell'Anno A, Danovaro R (2005) Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science, 309, 2179.
21. Denoyelle M, Jorissen FJ, Martin D, Galgani F, Miné J (2010) Comparison of benthic foraminifera and macrofaunal indicators of the impact of oil-based drill mud disposal. Marine Pollution Bulletin, 60, 2007-2021.
22. Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology: An Annual Review, 33, 245-303.
23. Edgcomb VP, Orsi W, Taylor GT et al. (2011) Accessing marine protists from the anoxic Cariaco Basin. The ISME Journal, 5, 1237-1241.
24. FAO (2012) The State of World Fisheries and Aquaculture 2012. Food and Agriculture Organization of the United Nations, Rome. ISBN 978-92-5-107225-7.
25. Fernandes TF, Eleftheriou A, Ackefors H et al. (2001) The scientific principles underlying the monitoring of the environmental impacts of aquaculture. Journal of Applied Ichthyology, 17, 181-193.
26. Frontalini F, Coccioni R (2011) Benthic foraminifera as bioindicators of pollution: a review of Italian research over the last three decades. Revue de Micropaléontologie, 54, 115-127.
27. Frontalini F, Buosi C, Da Pelo S et al. (2009) Benthic foraminifera as bio-indicators of trace element pollution in the heavily contaminated Santa Gilla lagoon (Cagliari, Italy). Marine Pollution Bulletin, 58, 858-877.
28. Gooday AJ (2002) Organic-walled allogromiids: aspects of their occurrence, diversity and ecology in marine habitats. Journal of Foraminiferal Research, 32, 384-399.
29. Gooday AJ, Anikeeva OV, Pawlowski J (2011) New genera and species of monothalamous Foraminifera from Bataclava and Kazach'ya Bays (Crimean Peninsula, Black Sea). Marine Biodiversity, 41, 481-494.
30. Hajibabaei M, Shokralla S, Zhou X, Singer GAC, Baird DJ (2011) Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS One, 6, e17497.
31. Hajibabaei M, Spall JL, Shokralla S, van Konynenburg S (2012) Assessing biodiversity of a freshwater benthic macroinvertebrate community through nondestructive environmental barcoding of DNA from preservative ethanol. BMC Ecology, 12, 28.
32. Höglund H (1947) Foraminifera in the Gullmar Fjord and the Skagerak. Zoologiska Bidrag från Uppsala, 26, 1-328.
33. Jones FC (2008) Taxonomic sufficiency: the influence of taxonomic resolution on freshwater bioassessments using benthic macroinvertebrates. Environmental Reviews, 16, 45-69.
34. Jorissen FJ, Bicchi E, Duchemin G et al. (2009) Impact of oil-based drill mud disposal on benthic foraminiferal assemblages on the continental margin off Angola. Deep Sea Research Part II: Topical Studies in Oceanography, 56, 2270-2291.
35. Kermarrec L, Franc A, Rimet F et al. (2013) Next-generation sequencing to inventory taxonomic diversity in eukaryotic communities: a test for freshwater diatoms. Molecular Ecology Resources, 13, 607-619.
36. Langlet D, Geslin E, Baal C et al. (2013) Foraminiferal survival after long-term in situ experimentally induced anoxia. Biogeosciences, 10, 7463-7480.
37. Lecroq B, Lejzerowicz F, Bachar D et al. (2011) Ultra-deep sequencing of foraminiferal microbarcodes unveils hidden richness of early monothalamous lineages in deep-sea sediments. Proceedings of the National Academy of Sciences, 108, 13177-13182.
38. Lejzerowicz F, Majewski M, Szczuciński W et al. (2013) Ancient DNA complements microfossil record in deep-sea subsurface sediments. Biology Letters, 9, 20130283.
39. Mojtahid M, Jorissen F, Pearson TH (2008) Comparison of benthic foraminiferal and macrofaunal responses to organic pollution in the Firth of Clyde (Scotland). Marine Pollution Bulletin, 56, 42-76.
40. Murray JW (2006) Ecology and Applications of Benthic Foraminifera. Cambridge University Press, Cambridge, 426 pp.
41. Novitsky JA (1986) Degradation of dead microbial biomass in a marine sediment. Applied and Environmental Microbiology, 52, 504-509.
42. Pawlowski J, Lecroq B (2010) Short rDNA barcodes for species identification in foraminifera. Journal of Eukaryotic Microbiology, 57, 197-205.
43. Pawlowski J, Majewski W (2011) Magnetite-bearing foraminifera from Admiralty Bay, West Antarctica, with description of Psammophaga magnetica, sp.nov. Journal of Foraminiferal Research, 41, 1-11.
44. Pawlowski J, Majewski W, Longet D et al. (2008) Genetic differentiation between Arctic and Antarctic monothalamous foraminifera. Polar Biology, 31, 1205-1216.
45. Pawlowski J, Audic S, Adl S et al. (2012) CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biology, 10, e1001419.
46. Sany SBT, Hashim R, Rezayi M, Salleh A, Safari O (2014) A review of strategies to monitor water and sediment quality for a sustainability assessment of marine environment. Environmental Science and Pollution Research, 21, 813-833.
47. Schönfeld J, Alve E, Geslin E et al. (2012) The FOBIMO (FOraminiferal BIo-MOnitoring) initiative-Towards a standardized protocol for soft-bottom benthic foraminiferal monitoring studies. Marine Micropaleontology, 94-95, 1-13.
48. Scott DB, Schafer CT, Honig C, Younger DC (1995) Temporal variations of benthic foraminiferal assemblages under or near aquaculture operations: documentation of impact history. Journal of Foraminiferal Research, 25, 224-235.
49. Shokralla S, Spall JL, Gibson JF, Hajibabaei M (2012) Next generation sequencing technologies for environmental DNA research. Molecular Ecology, 21, 1794-1805.
50. Stein ED, White BP, Mazor RD, Miller PE, Pilgrim EM (2013) Evaluating ethanol-based sample preparation to facilitate use of DNA barcoding in routine freshwater biomonitoring programs using benthic macroinvertebrates. PLoS One, 8, e51273.
51. Stoeck T, Zuendorf A, Breiner H-W, Behnke A (2007) A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microbial Ecology, 53, 328-339.
52. Stoeck TA, Behnke A, Christen R et al. (2009) Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities. BMC Biology, 7, 72.
53. Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Molecular Ecology, 21, 2045-2050.
54. Vidovic J, Cosovic V, Juracic M, Petricioli D (2009) Impact of fish farming on foraminiferal community, Drvenik Veliki Island, Adriatic Sea, Croatia. Marine Pollution Bulletin, 58, 1297-1309.
55. Wang J, McLenachan PA, Biggs PJ et al. (2013) Environmental bio-monitoring with high-throughput sequencing. Briefings in Bioinformatics, 14, 575-588.
56. Weber A, Pawlowski J (2013) Can abundance of protists be inferred from sequence data? A case study of cultured Foraminifera. PLoS One, 8, e56739.
57. Wilding TA (2012) Changes in sedimentary redox associated with mussel (Mytilus edulis L.) farms on the West-Coast of Scotland. PLoS One, 7, e45159.
58. Wilding TA, Sayer MDJ (2002) Evaluating artificial reef performance: approaches to pre- and post-deployment research. ICES Journal of Marine Science, 59, S222-S230.
59. Wilding TA, Cromey CJ, Nickell TD, Hughes DJ (2012) Salmon farm impacts on muddy-sediment megabenthic assemblages on the west coast of Scotland. Aquaculture Environment Interactions, 2, 145-156.
60. Wildish DJ, Hargrave BT, Pohle G (2001) Cost-effective monitoring of organic enrichment resulting from salmon mariculture. ICES Journal of Marine Science, 58, 469-476.
61. Wilson A, Magill S, Black KD (2009) Review of environmental impact assessment and monitoring in salmon aquaculture. In: Environmental Impact Assessment and Monitoring in Aquaculture (ed. FAO). FAO, Rome. FAO Fisheries and Aquaculture Technical Paper, 527, 455-535.
62. Yu DW, Ji Y, Emerson BC et al. (2012) Biodiversity soup: metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods in Ecology and Evolution, 3, 613-623.
63. Zhou X, Li Y, Liu S et al. (2013) Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. GigaScience, 2, 4.
64. Zobell CE (1946) Studies on redox potential of marine sediments. Bulletin of the American Association of Petrology and Geology, 30, 477-513.