Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

DNA barcoding and metabarcoding of highly diverse aquatic mites (Acarina) can improve their use in routine biological monitoring

Melissa E. Carew https://orcid.org/0000-0001-5833-6410 A B * , Wen Kyle Yow A , Katie L. Robinson A , Rhys A. Coleman C and Ary A. Hoffmann A
+ Author Affiliations
- Author Affiliations

A Pest and Environmental Adaptation Research Group (PEARG), School of BioSciences, Bio21 Institute, 30 Flemington Road, The University of Melbourne, Vic. 3010, Australia.

B Waterway Ecosystem Research Group (WERG), School of Ecosystem and Forestry Sciences, 500 Yarra Boulevard, Richmond, Vic. 3121, Australia.

C Applied Research, Melbourne Water, 990 La Trobe Street, Docklands, Vic. 3008, Australia.

* Correspondence to: mecarew@unimelb.edu.au

Handling Editor: Donald Baird

Marine and Freshwater Research 73(7) 900-914 https://doi.org/10.1071/MF21291
Submitted: 6 October 2021  Accepted: 7 April 2022   Published: 17 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: Acarina are commonly collected in macroinvertebrate surveys used to monitor freshwater ecosystems. However, they can be difficult to identify morphologically requiring considerable taxonomic skill for identification to finer taxonomic levels. Therefore, in biomonitoring they are identified to subclass despite high species diversity and varied environmental responses. DNA barcoding individuals and DNA metabarcoding of bulk samples enables species to be accurately and routinely identified. However, poor DNA barcode coverage of Australian aquatic mites has hampered their use in DNA studies.

Aims: Here, we aim to generate DNA barcodes for mites from Greater Melbourne, Australia.

Key results: For many specimens, we link DNA barcodes to genus-level morphological identifications using genetic analysis of DNA barcodes to understand biodiversity. We then test if new DNA barcodes can improve identification of mites in samples processed with DNA metabarcoding. We found Australian aquatic mites showed high diversity with many DNA barcodes represented by single specimens.

Conclusions: Increased mite DNA barcode library coverage improved their detection using DNA metabarcoding.

Implications: Given high species diversity, much effort will be required to improve DNA barcode coverage for aquatic mites in Australia and integrate barcodes with species level taxonomy, allowing Acarina to be better incorporated into DNA-based biological monitoring.

Keywords: Australia, biodiversity, freshwater, Halacaroidea, Hydracarina, macroinvertebrates, Mesostigmata, Oribatida, species identification.


References

Baird, DJ, and Hajibabaei, M (2012). Biomonitoring 2.0: a new paradigm in ecosystem assessment made possible by next-generation DNA sequencing. Molecular Ecology 21, 2039–2044.
Biomonitoring 2.0: a new paradigm in ecosystem assessment made possible by next-generation DNA sequencing.Crossref | GoogleScholarGoogle Scholar | 22590728PubMed |

Blattner, L, Gerecke, R, and von Fumetti, S (2019). Hidden biodiversity revealed by integrated morphology and genetic species delimitation of spring dwelling water mite species (Acari, Parasitengona: Hydrachnidia). Parasites & Vectors 12, 492.
Hidden biodiversity revealed by integrated morphology and genetic species delimitation of spring dwelling water mite species (Acari, Parasitengona: Hydrachnidia).Crossref | GoogleScholarGoogle Scholar |

Bolyen, E, Rideout, JR, Dillon, MR, et al. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852–857.
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.Crossref | GoogleScholarGoogle Scholar | 31341288PubMed |

Callahan, BJ, McMurdie, PJ, Rosen, MJ, Han, AW, Johnson, AJA, and Holmes, SP (2016). DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583.
DADA2: high-resolution sample inference from Illumina amplicon data.Crossref | GoogleScholarGoogle Scholar | 27214047PubMed |

Caporaso, JG, Kuczynski, J, Stombaugh, J, et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335–336.
QIIME allows analysis of high-throughput community sequencing data.Crossref | GoogleScholarGoogle Scholar | 20383131PubMed |

Carew, ME, and Hoffmann, AA (2015). Delineating closely related species with DNA barcodes for routine biological monitoring. Freshwater Biology 60, 1545–1560.
Delineating closely related species with DNA barcodes for routine biological monitoring.Crossref | GoogleScholarGoogle Scholar |

Carew, ME, Coleman, RA, and Hoffmann, AA (2018a). Can non-destructive DNA extraction of bulk invertebrate samples be used for metabarcoding? PeerJ 6, e4980.
Can non-destructive DNA extraction of bulk invertebrate samples be used for metabarcoding?Crossref | GoogleScholarGoogle Scholar | 29915700PubMed |

Carew, ME, Kellar, CR, Pettigrove, VJ, and Hoffmann, AA (2018b). Can high-throughput sequencing detect macroinvertebrate diversity for routine monitoring of an urban river? Ecological Indicators 85, 440–450.
Can high-throughput sequencing detect macroinvertebrate diversity for routine monitoring of an urban river?Crossref | GoogleScholarGoogle Scholar |

Carew ME, Hoffmann AA, Kellar CL, Stevenson K, Walsh CJ, Danger A, Coleman RA (2019) Integrating DNA metabarcoding into Melbourne Water’s macroinvertebrate monitoring program. Melbourne Water Corporation, Australia.

Carew, ME, Coleman, RA, Robinson, KL, and Hoffmann, AA (2021). Using unsorted sweep-net samples to rapidly assess macroinvertebrate biodiversity. Freshwater Science 40, 551–565.
Using unsorted sweep-net samples to rapidly assess macroinvertebrate biodiversity.Crossref | GoogleScholarGoogle Scholar |

Chessman, BC (1995). Rapid assessment of rivers using macroinvertebrates: a procedure based on habitat-specific sampling, family level identification and a biotic index. Austral Ecology 20, 122–129.
Rapid assessment of rivers using macroinvertebrates: a procedure based on habitat-specific sampling, family level identification and a biotic index.Crossref | GoogleScholarGoogle Scholar |

Colloff MJ, Halliday RB (1998) ‘Oribatid mites: a catalogue of Australian genera and species.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Di Sabatino, A, Smit, H, Gerecke, R, Goldschmidt, T, Matsumoto, N, and Cicolani, B (2007). Global diversity of water mites (Acari, Hydrachnidia; Arachnida) in freshwater. Hydrobiologia 595, 303–315.
Global diversity of water mites (Acari, Hydrachnidia; Arachnida) in freshwater.Crossref | GoogleScholarGoogle Scholar |

Drummond, AJ, Suchard, MA, Xie, D, and Rambaut, A (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.Crossref | GoogleScholarGoogle Scholar | 22367748PubMed |

Elbrecht, V, and Leese, F (2017). Validation and development of COI metabarcoding primers for freshwater macroinvertebrate bioassessment. Frontiers in Environmental Science 5, 11.
Validation and development of COI metabarcoding primers for freshwater macroinvertebrate bioassessment.Crossref | GoogleScholarGoogle Scholar |

Elbrecht, V, and Steinke, D (2019). Scaling up DNA metabarcoding for freshwater macrozoobenthos monitoring. Freshwater Biology 64, 380–387.
Scaling up DNA metabarcoding for freshwater macrozoobenthos monitoring.Crossref | GoogleScholarGoogle Scholar |

EPA Victoria (2021) Guidelines for environmental management; water. Available at https://www.epa.vic.gov.au/about-epa/publications/604-2 [Verified 9 October 2021]

Folmer, O, Black, M, Hoeh, W, Lutz, R, and Vrijenhoek, R (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 7881515PubMed |

Glowska, E, Dragun-Damian, A, Broda, L, Dabert, J, and Dabert, M (2014). DNA barcodes reveal female dimorphism in syringophilid mites (Actinotrichida: Prostigmata: Cheyletoidea): Stibarokris phoeniconaias and Ciconichenophilus phoeniconaias are conspecific. Folia Parasitologica 61, 272–276.
DNA barcodes reveal female dimorphism in syringophilid mites (Actinotrichida: Prostigmata: Cheyletoidea): Stibarokris phoeniconaias and Ciconichenophilus phoeniconaias are conspecific.Crossref | GoogleScholarGoogle Scholar | 25065134PubMed |

Goldschmidt, T (2016). Water mites (Acari, Hydrachnidia): powerful but widely neglected bioindicators – a review. Neotropical Biodiversity 2, 12–25.
Water mites (Acari, Hydrachnidia): powerful but widely neglected bioindicators – a review.Crossref | GoogleScholarGoogle Scholar |

Goldschmidt, T, Helson, JE, and Williams, DD (2016). Ecology of water mite assemblages in Panama – first data on water mites (Acari, Hydrachnidia) as bioindicators in the assessment of biological integrity of neotropical streams. Limnologica 59, 63–77.
Ecology of water mite assemblages in Panama – first data on water mites (Acari, Hydrachnidia) as bioindicators in the assessment of biological integrity of neotropical streams.Crossref | GoogleScholarGoogle Scholar |

Growns JE (2001) Aquatic mites as bioindicators, with an Australian example. In ‘Acarology: proceedings of the 10th international congress’, 5–10 July 1998, Canberra, ACT, Australia. (Eds DE Walter, RB Halliday, HC Proctor, RA Norton, MJ Colloff) pp. 136. (CSIRO Publishing: Melbourne, Vic., Australia)

Hajibabaei, M, Shokralla, S, Zhou, X, Singer, GAC, and Baird, DJ (2011). Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS ONE 6, e17497.
Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos.Crossref | GoogleScholarGoogle Scholar | 21533287PubMed |

Hajibabaei, M, Spall, JL, Shokralla, S, and van Konynenburg, S (2012). Assessing biodiversity of a freshwater benthic macroinvertebrate community through non-destructive environmental barcoding of DNA from preservative ethanol. BMC Ecology 12, 28.
Assessing biodiversity of a freshwater benthic macroinvertebrate community through non-destructive environmental barcoding of DNA from preservative ethanol.Crossref | GoogleScholarGoogle Scholar | 23259585PubMed |

Harvey, MS (1989). Pezidae, a new freshwater mite family from Australia (Acarina: Halacaroidea). Invertebrate Systematics 3, 771–781.
Pezidae, a new freshwater mite family from Australia (Acarina: Halacaroidea).Crossref | GoogleScholarGoogle Scholar |

Harvey, MS (1996). A review of the water mite family Pionidae in Australia (Acarina: Hygrobatoidea). Records of the Western Australian Museum 17, 361–393.

Harvey MS (1998) ‘Australian water mites: a guide to families and genera.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Hebert, PDN, Cywinska, A, Ball, SL, and deWaard, JR (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London – B. Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.Crossref | GoogleScholarGoogle Scholar |

Hebert, PDN, Penton, EH, Burns, JM, Janzen, DH, and Hallwachs, W (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.
Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar |

Jackson, JK, Battle, JM, White, BP, Pilgrim, EM, Stein, ED, Miller, PE, and Sweeney, BW (2014). Cryptic biodiversity in streams: a comparison of macroinvertebrate communities based on morphological and DNA barcode identifications. Freshwater Science 33, 312–324.
Cryptic biodiversity in streams: a comparison of macroinvertebrate communities based on morphological and DNA barcode identifications.Crossref | GoogleScholarGoogle Scholar |

Leray, M, Yang, JY, Meyer, CP, Mills, SC, Agudelo, N, Ranwez, V, Boehm, JT, and Machida, RJ (2013). A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Frontiers in Zoology 10, 34.
A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents.Crossref | GoogleScholarGoogle Scholar | 23767809PubMed |

Martin, M (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17, 10–12.
Cutadapt removes adapter sequences from high-throughput sequencing reads.Crossref | GoogleScholarGoogle Scholar |

Miccoli, FP, Lombardo, P, and Cicolani, B (2013). Indicator value of lotic water mites (Acari: Hydrachnidia) and their use in macroinvertebrate-based indices for water quality assessment purposes. Knowledge and Management of Aquatic Ecosystems 411, 08.
Indicator value of lotic water mites (Acari: Hydrachnidia) and their use in macroinvertebrate-based indices for water quality assessment purposes.Crossref | GoogleScholarGoogle Scholar |

Monaghan, MT, Wild, R, Elliot, M, et al. (2009). Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58, 298–311.
Accelerated species inventory on Madagascar using coalescent-based models of species delineation.Crossref | GoogleScholarGoogle Scholar | 20525585PubMed |

Montes-Ortiz, L, and Elías-Gutiérrez, M (2020). Water mite diversity (Acariformes: Prostigmata: Parasitengonina: Hydrachnidiae) from Karst ecosystems in southern of Mexico: a barcoding approach. Diversity 12, 329.
Water mite diversity (Acariformes: Prostigmata: Parasitengonina: Hydrachnidiae) from Karst ecosystems in southern of Mexico: a barcoding approach.Crossref | GoogleScholarGoogle Scholar |

Pons, J, Barraclough, TG, Gomez-Zurita, J, Cardoso, A, Duran, DP, Hazell, S, Kamoun, S, Sumlin, WD, and Vogler, AP (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.
Sequence-based species delimitation for the DNA taxonomy of undescribed insects.Crossref | GoogleScholarGoogle Scholar | 16967577PubMed |

Porter, TM, and Hajibabaei, M (2018). Scaling up: a guide to high-throughput genomic approaches for biodiversity analysis. Molecular Ecology 27, 313–338.
Scaling up: a guide to high-throughput genomic approaches for biodiversity analysis.Crossref | GoogleScholarGoogle Scholar | 29292539PubMed |

Proctor HC (2007) Aquatic mites in assessment of stream invertebrate diversity. In ‘Acarology XI: proceedings of the international congress’, 8–13 September 2002, Coyoacán, Mexico City. (Eds JB Morales-Malacara, V Behan-Pelletier, E Ueckermann, TM Peréz, EG Estrada-Venegas, M Badii) pp. 105–117. (Instituto de Biología and Facultad de Ciencias, Universidad Nacional Autónoma de México; Sociedad Latinoamericana de Acarología)

Proctor HC, Smith IM, Cook DR, Smith BP (2015) Chapter 25 – Subphylum Chelicerata, class Arachnida. In ‘Thorp and Covich’s freshwater invertebrates’, 4th edn. (Eds JH Thorp, DC Rogers) pp. 599–660. (Academic Press: Boston, MA, USA)

Puillandre, N, Modica, MV, Zhang, Y, Sirovich, L, Boisselier, M-C, Cruaud, C, Holford, M, and Samadi, S (2012). Large-scale species delimitation method for hyperdiverse groups. Molecular Ecology 21, 2671–2691.
Large-scale species delimitation method for hyperdiverse groups.Crossref | GoogleScholarGoogle Scholar | 22494453PubMed |

Ratnasingham, S, and Hebert, PDN (2013). A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE 8, e66213.
A DNA-based registry for all animal species: the barcode index number (BIN) system.Crossref | GoogleScholarGoogle Scholar | 23861743PubMed |

Schatz H, Behan-Pelletier V (2008) Global diversity of oribatids (Oribatida: Acari: Arachnida). In ‘Freshwater animal diversity assessment’. (Eds EV Balian, C Lévêque, H Segers, K Martens) pp. 323–328. (Springer Netherlands: Dordrecht, Netherlands)

Shokralla, S, Porter, TM, Gibson, JF, Dobosz, R, Janzen, DH, Hallwachs, W, Golding, GB, and Hajibabaei, M (2015). Massively parallel multiplex DNA sequencing for specimen identification using an Illumina MiSeq platform. Scientific Reports 5, 9687.
Massively parallel multiplex DNA sequencing for specimen identification using an Illumina MiSeq platform.Crossref | GoogleScholarGoogle Scholar | 25884109PubMed |

Simpson JC, Norris RH (2000) Biological assessment of river quality: development of AUSRIVAS models and outputs. In ‘Assessing the biological quality of fresh waters RIVPACS and other techniques’. (Eds JF Wright, DW Sutcliffe, MT Furse) pp. 125–142. (Freshwater Biological Association, The Ferry House: Far Sawrey, Ambleside, UK)

Smit, H (2010). Australian water mites of the subfamily Notoaturinae Besch (Acari: Hydrachnidia: Aturidae), with the description of 24 new species. International Journal of Acarology 36, 101–146.
Australian water mites of the subfamily Notoaturinae Besch (Acari: Hydrachnidia: Aturidae), with the description of 24 new species.Crossref | GoogleScholarGoogle Scholar |

Stålstedt, J, Bergsten, J, and Ronquist, F (2013). “Forms” of water mites (Acari: Hydrachnidia): intraspecific variation or valid species? Ecology and Evolution 3, 3415–3435.
“Forms” of water mites (Acari: Hydrachnidia): intraspecific variation or valid species?Crossref | GoogleScholarGoogle Scholar | 24223279PubMed |

Thompson, JD, Plewniak, F, and Poch, O (1999). A comprehensive comparison of multiple sequence alignment programs. Nucleic Acids Research 27, 2682–2690.
A comprehensive comparison of multiple sequence alignment programs.Crossref | GoogleScholarGoogle Scholar | 10373585PubMed |

Vasquez, AA, Qazazi, MS, Fisher, JR, Failla, AJ, Rama, S, and Ram, JL (2017). New molecular barcodes of water mites (Trombidiformes: Hydrachnidiae) from the Toledo Harbor region of Western Lake Erie, USA, with first barcodes for Krendowskia (Krendowskiidae) and Koenikea (Unionicolidae). International Journal of Acarology 43, 494–498.
New molecular barcodes of water mites (Trombidiformes: Hydrachnidiae) from the Toledo Harbor region of Western Lake Erie, USA, with first barcodes for Krendowskia (Krendowskiidae) and Koenikea (Unionicolidae).Crossref | GoogleScholarGoogle Scholar |

Viets, KO (1978). New water mites (Hydrachnellae: Acari) from Australia. Marine and Freshwater Research 29, 77–92.
New water mites (Hydrachnellae: Acari) from Australia.Crossref | GoogleScholarGoogle Scholar |

Vuataz, L, Sartori, M, Wagner, A, and Monaghan, MT (2011). Toward a DNA taxonomy of alpine Rhithrogena (Ephemeroptera: Heptageniidae) using a mixed Yule-coalescent analysis of mitochondrial and nuclear DNA. PLoS ONE 6, e19728.
Toward a DNA taxonomy of alpine Rhithrogena (Ephemeroptera: Heptageniidae) using a mixed Yule-coalescent analysis of mitochondrial and nuclear DNA.Crossref | GoogleScholarGoogle Scholar | 21611178PubMed |

Walsh, CJ (1997). A multivariate method for determining optimal subsample size in the analysis of macroinvertebrate samples. Marine and Freshwater Research 48, 241–248.
A multivariate method for determining optimal subsample size in the analysis of macroinvertebrate samples.Crossref | GoogleScholarGoogle Scholar |

Walsh, CJ, and Kunapo, J (2009). The importance of upland flow paths in determining urban effects on stream ecosystems. Journal of the North American Benthological Society 28, 977–990.
The importance of upland flow paths in determining urban effects on stream ecosystems.Crossref | GoogleScholarGoogle Scholar |

Walsh, CJ, and Webb, JA (2014). Spatial weighting of land use and temporal weighting of antecedent discharge improves prediction of stream condition. Landscape Ecology 29, 1171–1185.
Spatial weighting of land use and temporal weighting of antecedent discharge improves prediction of stream condition.Crossref | GoogleScholarGoogle Scholar |

Walter DE, Proctor HC (2013) Acari underwater, or, why did mites take the plunge? In ‘Mites: ecology, evolution and behaviour’. (Eds DE Walter, HC Proctor) pp. 229–280. (Springer Netherlands: Dordrecht, Netherlands)

Weigand, H, Beermann, AJ, Čiampor, F, et al. (2019). DNA barcode reference libraries for the monitoring of aquatic biota in Europe: gap-analysis and recommendations for future work. Science of the Total Environment 678, 499–524.
DNA barcode reference libraries for the monitoring of aquatic biota in Europe: gap-analysis and recommendations for future work.Crossref | GoogleScholarGoogle Scholar | 31077928PubMed |

Więcek, M, Broda, Ł, Proctor, H, Dabert, M, Smith, BP, and Dabert, J (2021). Species boundaries among extremely diverse and sexually dimorphic, Arrenurus, water mites (Acariformes: Hydrachnidiae: Arrenuridae). bioRxiv , 2021.04.04.438411.
Species boundaries among extremely diverse and sexually dimorphic, Arrenurus, water mites (Acariformes: Hydrachnidiae: Arrenuridae).Crossref | GoogleScholarGoogle Scholar |

Young, MR, Behan-Pelletier, VM, and Hebert, PDN (2012). Revealing the hyperdiverse mite fauna of subarctic Canada through DNA barcoding. PLoS ONE 7, e48755.
Revealing the hyperdiverse mite fauna of subarctic Canada through DNA barcoding.Crossref | GoogleScholarGoogle Scholar | 23133656PubMed |

Young, MR, Proctor, HC, deWaard, JR, and Hebert, PDN (2019). DNA barcodes expose unexpected diversity in Canadian mites. Molecular Ecology 28, 5347–5359.
DNA barcodes expose unexpected diversity in Canadian mites.Crossref | GoogleScholarGoogle Scholar | 31674085PubMed |

Yu, DW, Ji, Y, Emerson, BC, Wang, X, Ye, C, Yang, C, and Ding, Z (2012). Biodiversity soup: metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods in Ecology and Evolution 3, 613–623.
Biodiversity soup: metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring.Crossref | GoogleScholarGoogle Scholar |

Zawal, A, Stryjecki, R, Stępień, E, Buczyńska, E, Buczyński, P, Czachorowski, S, Pakulnicka, J, and Śmietana, P (2017). The influence of environmental factors on water mite assemblages (Acari, Hydrachnidia) in a small lowland river: an analysis at different levels of organization of the environment. Limnology 18, 333–343.
The influence of environmental factors on water mite assemblages (Acari, Hydrachnidia) in a small lowland river: an analysis at different levels of organization of the environment.Crossref | GoogleScholarGoogle Scholar |