Barcoding diatoms: evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols

  • Jonas Zimmermann
  • Regine Jahn
  • Birgit Gemeinholzer
Original Article

Abstract

Diatoms are present in all types of water bodies and their species diversity is influenced greatly by environmental conditions. This means that diatom occurrence and abundances are suitable indicators of water quality. Furthermore, continuous screening of algal biodiversity can provide information about diversity changes in ecosystems. Thus, diatoms represent a desirable group for which to develop an easy to use, quick, efficient, and standardised organism identification tool to serve routine water quality assessments. Because conventional morphological identification of diatoms demands specialised in-depth knowledge, we have established standard laboratory procedures for DNA barcoding in diatoms. We (1) identified a short segment (about 400 bp) of the SSU (18S) rRNA gene which is applicable for the identification of diatom taxa, and (2) elaborated a routine protocol including standard primers for this group of microalgae. To test the universality of the primer binding sites and the discriminatory power of the proposed barcode region, 123 taxa, representing limnic diatom diversity, were included in the study and identified at species level. The effectiveness of the barcode was also scrutinised within a closely related species group, namely the Sellaphora pupula taxon complex and relatives.

Keywords

18S (SSU) rRNA gene Bacillariophyta DNA barcoding Diatoms Standard laboratory procedure 

References

  1. Alverson, A. J., Cannone, J. J., Gutell, R. R., & Theriot, E. C. (2006). The evolution of elongate shape in diatoms. Journal of Phycology, 42, 655–668.CrossRefGoogle Scholar
  2. Archibald, R. E. M. (1984). Diatom illustrations—an appeal. Bacillaria, 7, 173–178.Google Scholar
  3. Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martinez, D., Putnam, N. H., et al. (2004). The genome of Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science, 306, 79–86.PubMedCrossRefGoogle Scholar
  4. Babanazarova, O. V., Likhoshway, Y. V., & Sherbakov, D. Y. (1996). On the morphological variability of Aulacoseira baicalensis and Aulacoseira islandica (Bacillariophyto) of Lake Baikal, Russia. Phycologia, 35, 113–123.CrossRefGoogle Scholar
  5. Bailey-Watts, A. E. (1976). Planktonic diatoms and some diatom-silica relations in a shallow eutrophic Scottish loch. Freshwater Biology, 6, 69–80.CrossRefGoogle Scholar
  6. Barth, D., Krenek, S., Fokin, S. I., & Berendonk, T. (2006). Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. Journal of Eukaryotic Microbiology, 53, 20–25.PubMedCrossRefGoogle Scholar
  7. Behnke, A., Friedl, T., Chepurnov, V. A., & Mann, D. G. (2004). Reproductive compatibility and rDNA sequence analyses in the Sellaphora pupula species complex (Bacillariophyta). Journal of Phycology, 40, 193–208.CrossRefGoogle Scholar
  8. Bellemain, E., Carlsen, T., Brochmann, C., Coissac, E., Taberlet, P., & Kauserud, H. (2010). ITS as an environmental DNA barcode for fungi: An in silico approach reveals potential PCR biases. BMC Microbiology, 10, 189. doi:10.1186/1471-2180-10-189.PubMedCrossRefGoogle Scholar
  9. Beszteri, B., Acs, E., Makk, J., Kovács, G., Márialigeti, K., & Kiss, K. T. (2001). Phylogeny of six naviculoid diatoms based on 18S rDNA sequences. International Journal of Systematic and Evolutionary Microbiology, 51, 1581–1586.PubMedGoogle Scholar
  10. Beszteri, B., Ács, É., & Medlin, L. K. (2005a). Conventional and geometric morphometric studies of valve ultrastructural variation in two closely related Cyclotella species (Bacillariophyta). European Journal of Phycology, 40, 89–103.CrossRefGoogle Scholar
  11. Beszteri, B., Ács, É., & Medlin, L. K. (2005b). Ribosomal DNA sequence variation among sympatric strains of the Cyclotella meneghiniana complex (Bacillariophyceae) reveals cryptic diversity. Protist, 156, 317–333.PubMedCrossRefGoogle Scholar
  12. Beszteri, B., John, U., & Medlin, L. K. (2007). An assessment of cryptic genetic diversity within the Cyclotella meneghiniana species complex (Bacillariophyta) based on nuclear and plastid genes, and amplified fragment length polymorphism. European Journal of Phycology, 42, 47–60.CrossRefGoogle Scholar
  13. Bhadury, P., Austen, M. C., Bilton, D. T., Lambshead, P. J. D., Rogers, A. D., & Smerdon, G. R. (2006). Development and evaluation of a DNA-barcoding approach for the rapid identification of nematodes. Marine Ecology Progress Series, 320, 1–9.CrossRefGoogle Scholar
  14. Blaxter, M. L. (2004). The promise of a DNA taxonomy. Philosophical Transactions of the Royal Society of London, Biological Sciences, 359, 669–679.CrossRefGoogle Scholar
  15. Blaxter, M., Elsworth, B., & Daub, J. (2004). DNA taxonomy of a neglected animal phylum: An unexpected diversity of tardigrades. Proceedings of the Royal Society of London, Biological Sciences, 271, 189–192.CrossRefGoogle Scholar
  16. Bowler, C., Allen, A. E., Badger, J. H., Grimwood, J., Jabbari, K., Kuo, A., et al. (2008). The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature, 456, 239–244.PubMedCrossRefGoogle Scholar
  17. Casteleyn, G., Adams, N. G., Vanormelingen, P., Debeer, A. E., Sabbe, K., & Vyverman, W. (2009). Natural hybrids in the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae): Genetic and morphological evidence. Protist, 160, 343–354.PubMedCrossRefGoogle Scholar
  18. Chantangsi, C., Lynn, D. H., Brandl, M. T., Cole, J. C., Hetrick, N., & Ikonomi, P. (2007). Barcoding ciliates: A comprehensive study of 75 isolates of the genus Tetrahynema. International Journal of Systematic and Evolutionary Microbiology, 57, 2412–2425.PubMedCrossRefGoogle Scholar
  19. Chase, M. W., Cowan, R. S., Hollingsworth, P. M., van den Berg, C., Madriñán, S., Petersen, G., et al. (2007). A proposal for a standardised protocol to barcode all land plants. Taxon, 56, 295–299.Google Scholar
  20. Cowan, R. S., Chase, M. W., Kress, W. J., & Savolainen, V. (2006). 300,000 species to identify: Problems, progress, and prospects in DNA barcoding of land plants. Taxon, 55, 611–616.CrossRefGoogle Scholar
  21. Cywinska, A., Hunter, F. F., & Hebert, P. D. N. (2006). Identifying Canadian mosquito species through DNA barcodes. Medical and Veterinary Entomology, 20, 413–424.PubMedCrossRefGoogle Scholar
  22. Ehara, M., Watanabe, K. I., & Ohama, T. (2000). Distribution of cognates of group II introns detected in mitochondrial cox1 genes of a diatom and haptophyte. Gene, 256, 157–167.PubMedCrossRefGoogle Scholar
  23. Erickson, D. L., Spouge, J., Resch, A., Weigt, L. A., & Kress, W. J. (2008). DNA barcoding in landplants: Developing standards to quantify and maximise success. Taxon, 57, 1304–1316.PubMedGoogle Scholar
  24. Evans, K. M., Wortley, A. H., & Mann, D. G. (2007). An assessment of potential diatom “barcode” genes (cox1, rbcL, 18S and ITS rDNA) and their effectiveness in determining relationships in Sellaphora (Bacillariophyta). Protist, 158, 349–364.PubMedCrossRefGoogle Scholar
  25. Evans, K. M., Wortley, A. H., Simpson, G. E., Chepurnov, V. A., & Mann, D. G. (2008). A molecular systematic approach to explore diversity within the Sellaphora pupula species complex (Bacillariophyta). Journal of Phycology, 44, 215–231.CrossRefGoogle Scholar
  26. Falkowski, P. G., Barber, R. T., & Smetacek, V. (1998). Biogeochemical controls and feedbacks on ocean primary production. Science, 281, 200–207.PubMedCrossRefGoogle Scholar
  27. Fazekas, A. J., Burgess, K. S., Kesanakurti, P. R., Graham, S. W., Newmaster, S. G., Husband, B. C., et al. (2008). Multiple multilocus DNA barcodes from the plastid genome discriminate plant species equally well. PloS One, 3(7), e2802. doi:10.1371/journal.pone.0002802.PubMedCrossRefGoogle Scholar
  28. Ferrell, J., & Beaton, M. (2007). The evaluation of DNA barcoding for identification of dinoflagellates: A test using Prorocentrum. In: Canadian barcode of life network 2007 science symposium (pp. 37). Guelph: Blackwell.Google Scholar
  29. Field, C. B., Behrenfeld, M. J., Randerson, J. T., & Falkowski, P. G. (1998). Primary production of the biosphere: Integrating terrestrial and oceanic components. Science, 281, 237–240.PubMedCrossRefGoogle Scholar
  30. Floyd, R., Abebe, E., Papert, A., & Blaxter, M. L. (2002). Molecular barcodes for soil nematode identification. Molecular Ecology, 11, 839–850.PubMedCrossRefGoogle Scholar
  31. Friedl, T., & O’Kelly, C. J. (2002). Phylogenetic relationships of green algae assigned to the genus Planophila (Chlorophyta): Evidence from 18S rDNA sequence data and ultrastructure. European Journal of Phycology, 37, 373–384.CrossRefGoogle Scholar
  32. Gemeinholzer, B., Oberprieler, C., & Bachman, K. (2006). Using GenBank data for plant identification: Possibilities and limitations using the ITS1 of Asteraceae species belonging to the tribes Lactuceae and Anthemideae. Taxon, 55, 173–187.CrossRefGoogle Scholar
  33. Gillespie, J. J., Johnston, J. F., Cannone, J., & Gutell, R. R. (2006). Characteristics of the nuclear (18S, 5.8S, 28S and 5S) and mitochondrial (12S and 16S) rRNA genes of Apis mellifera (Insecta: Hymenoptera): Structure, organization, and retrotransposable elements. Insect Molecular Biology, 15, 657–686.PubMedCrossRefGoogle Scholar
  34. Guillard, R. R. L., & Lorenzen, C. J. (1972). Yellow green algae with chlorophyllide. Journal of Phycology, 8, 10–14.Google Scholar
  35. Hajibabaei, M., Janzen, D. H., Burns, J. M., Hallwachs, W., & Hebert, P. D. N. (2006). DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the USA, 103, 968–971.PubMedCrossRefGoogle Scholar
  36. Hajibabaei, M., Smith, A., Janzen, D. H., Rodriguez, J. J., Whitfield, J. B., & Hebert, P. D. N. (2006). A minimalist barcode can identify specimens whose DNA is degraded. Molecular Ecology, 6, 959–964.CrossRefGoogle Scholar
  37. Hajibabaei, M., Singer, G. A. C., Hebert, P. D. N., & Hickey, D. A. (2007). DNA barcoding: How it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics, 23, 167–172.PubMedCrossRefGoogle Scholar
  38. Håkansson, H., & Kling, H. (1989). A light and electron microscope study of previously described and new Stephanodiscus species (Bacillariophyceae) from central and northern Canadian lakes, with ecological notes on the species. Diatom Research, 4, 269–288.Google Scholar
  39. Håkansson, H., & Kling, H. (1990). The current status of some very small freshwater diatoms of the genera Stephanodiscus and Cyclostephanos. Diatom Research, 5, 273–287.Google Scholar
  40. Hall, T. A. (1999). BioEdit: A user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleid Acids Symposium Series, 41, 95–98.Google Scholar
  41. Hamsher, S. E., Evans, K. M., Mann, D. G., Poulíčková, A., & Saunders, G. W. (2011). Barcoding diatoms: Exploring alternatives to COI-5P. Protist, 162, 405–422.PubMedCrossRefGoogle Scholar
  42. Hebert, P. D. N., Cywinska, A., Ball, S. L., & de Waard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Biological Sciences, 270, 313–321.CrossRefGoogle Scholar
  43. Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S., & Francis, C. M. (2004). Identification of birds through DNA barcodes. PLoS Biology, 2, 1657–1663.CrossRefGoogle Scholar
  44. Hickerson, M. J., Meyer, C. P., & Moritz, C. (2006). DNA barcoding will often fail to discover new animal species over broad parameter space. Systematic Biology, 55, 729–739.PubMedCrossRefGoogle Scholar
  45. Hollingsworth, M. L., Clark, A. A., Forrest, L. L., Richardson, J., Pennington, R. T., Long, D. G., et al. (2009). Selecting barcoding loci for plants: Evaluation of seven candidate loci with species-level sampling in three divergent groups of land plants. Molecular Ecology Resources, 9, 439–457.PubMedCrossRefGoogle Scholar
  46. Huang, J., Xu, Q., Sun, Z. J., Tang, G. L., & Su, Z. Y. (2007). Identifying earthworms through DNA barcodes. Pedobiologia, 51, 301–309.CrossRefGoogle Scholar
  47. Huber, J. A., Morrison, H. G., Huse, S. M., Neal, P. R., Sogin, M. L., & Welch, D. M. (2009). Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environmental Microbiology, 11, 1292–1302.PubMedCrossRefGoogle Scholar
  48. Huse, S. M., Huber, J. A., Morrison, H. G., Sogin, M. L., & Welch, D. M. (2007). Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biology, 8, R143.PubMedCrossRefGoogle Scholar
  49. Imanian, B., Carpenter, K. J., & Keeling, P. J. (2007). Mitochondrial genome of a tertiary endosymbiont retains genes for electron transport proteins. Journal of Eukaryotic Microbiology, 54, 146–153.PubMedCrossRefGoogle Scholar
  50. Ivanova, N. V., Zemlak, T. S., Hanner, R. H., & Hebert, P. D. N. (2007). Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes, 7, 544–548.CrossRefGoogle Scholar
  51. Jahn, R. (1986). A study of Gomphonema augur Ehrenberg: The structure of the frustule and its variability in clones and populations. In M. Ricard (Ed.), Proceedings of the 8th International Diatom Symposium 1984 (pp. 191–204). Paris: Koeltz Scientific Books.Google Scholar
  52. Jahn, R., & Kusber, W. H. (2002+). AlgaTerra Information System (online). Botanic Garden and Botanical Museum Berlin-Dahlem, Freie Universität Berlin. http://www.algaterra.org. Accessed 30 December 2010.
  53. Jahn, R., Zetzsche, H., Reinhardt, R., & Gemeinholzer, B. (2007). Diatoms and DNA barcoding: A pilot study on an environmental sample. In W. H. Kusber & R. Jahn (Eds.), Proceedings of the 1st Central European Diatom Meeting 2007 (pp. 63–68). Berlin: Botanic Garden and Botanical Museum Berlin-Dahlem.CrossRefGoogle Scholar
  54. Jensen, K. G., Moestrup, Ø., & Schmid, A. M. M. (2003). Ultrastructure of the male gametes from two centric diatoms, Chaetoceros laciniosus and Coscinodiscus wailesii (Bacillariophyceae). Phycologia, 42, 98–105.CrossRefGoogle Scholar
  55. Kane, R. A., Stothard, J. R., Emery, A. M., & Rollinson, D. (2008). Molecular characterization of freshwater snails in the genus Bulinus: a role for barcodes? Parasites & Vectors, 1(15). doi:10.1186/1756-3305-1-15.
  56. Kelly, L. J., Ameka, G. K., & Chase, M. W. (2010). DNA barcoding of African Podostemaceae (river-weeds): A test of proposed barcode regions. Taxon, 10, 251–260.Google Scholar
  57. Kobayasi, H., Kobayashi, H., & Idei, M. (1985). Fine structure and taxonomy of the small and tiny Stephanodiscus (Bacillariophyceae) species in Japan. 3. Co-occurrence of Stephanodiscus minutulus (Kütz.) Round and S. parvus Stoerm. & Håk. Japanese Journal of Phycology, 33, 293–300.Google Scholar
  58. Kooistra, W. H. C. F., & Medlin, L. K. (1996). Evolution of the diatoms (Bacillariophyta): IV. A reconstruction of their age from small subunit rRNA coding regions and the fossil record. Molecular Phylogenetics and Evolution, 6, 391–407.PubMedCrossRefGoogle Scholar
  59. Kress, W. J., & Erickson, D. L. (2007). A two-locus global DNA barcode for landplants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS Biology, 2, e508. doi:10.1371/journal.pone.0000508.Google Scholar
  60. Kress, W. J., Wurdack, K. J., Zimmer, E. A., Weigt, L. A., & Janzen, D. H. (2005). Use of DNA barcodes to identify flowering plants. Proceedings of the National Academy of Sciences of the USA, 102, 8369–8374.PubMedCrossRefGoogle Scholar
  61. Kucera, H., & Saunders, G. W. (2008). Assigning morphological variance of Fucus (Fucales, Phaeophyceae) in Canadian waters to recognized species using DNA barcoding. Botany, 86, 1065–1079.CrossRefGoogle Scholar
  62. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.PubMedCrossRefGoogle Scholar
  63. Lefèvre, E., Bardot, C., Noёl, C., Carrias, J., Viscogliosi, C., Amblard, C., et al. (2007). Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: Evidence from a molecular diversity study in a deep meromictic lake. Environmental Microbiology, 9, 61–71.PubMedCrossRefGoogle Scholar
  64. Levialdi Ghiron, J. H., Amato, A., Montresor, M., & Kooistra, W. H. C. F. (2008). Plastid inheritance in the planctonic raphid pennate Pseudo-nitzschia delicatissima (Bacillariophyceae). Protist, 159, 91–98.PubMedCrossRefGoogle Scholar
  65. Lewis, L. A., & Flechtner, V. R. (2004). Cryptic species of Scenedesmus (Chlorophyta) from desert soil communities of western North America. Journal of Phycology, 40, 1127–1137.CrossRefGoogle Scholar
  66. Liao, P. C., Huang, B. H., & Huang, S. (2007). Microbial community composition of the Danshui River estuary of northern Taiwan and the practicality of the phylogenetic method in microbial barcoding. Microbial Ecology, 54, 497–507.PubMedCrossRefGoogle Scholar
  67. Litaker, R. W., Vandersea, M. W., Kibler, S. R., Reece, K. S., Stokes, N. A., Lutzoni, F. M., et al. (2007). Recognizing dinoflagellate species using ITS rDNA sequences. Journal of Phycology, 43, 344–355.CrossRefGoogle Scholar
  68. Lynn, D. H., & Strüder-Kypke, M. C. (2006). Species of Tetrahymena identical by small subunit rRNA gene sequences are discriminated by mitochondrial cytochrome c oxidase I gene sequences. Journal of Eukaryotic Microbiology, 53, 385–387.PubMedCrossRefGoogle Scholar
  69. Mann, D. G. (1999). The species concept in diatoms. Phycologia, 38, 437–495.CrossRefGoogle Scholar
  70. McManus, H. A., & Lewis, L. A. (2005). Molecular phylogenetics, morphological variation, and colony-form evolution in the family Hydrodictyaceae (Sphaeropleales, Chlorophyta). Phycologia, 44, 582–595.CrossRefGoogle Scholar
  71. Medlin, L. K., & Kaczmarska, I. (2004). Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia, 43, 245–270.CrossRefGoogle Scholar
  72. Medlin, L. K., Elwood, H. J., Stickel, S., & Sogin, M. L. (1991). Morphological and genetic variation within the diatom Skeletonema costatum (Bacillariophyta): Evidence for a new species, Skeletonema pseudocostatum. Journal of Phycology, 27, 514–524.CrossRefGoogle Scholar
  73. Medlin, L. K., Kooistra, W. H., Gersonde, R., & Wellbrock, U. (1996). Evolution of the diatoms (Bacillariophyta). II. Nuclear-encoded small subunit rRNA sequence comparisons confirm a paraphyletic origin for the centric diatoms. Molecular Biology and Evolution, 13, 67–75.PubMedGoogle Scholar
  74. Messing, J. (1983). New M13 vectors for cloning. Methods in Enzymology, 101, 20–78.PubMedCrossRefGoogle Scholar
  75. Meyer, C. P., & Paulay, G. (2005). DNA barcoding: Error rates based on comprehensive sampling. PLoS Biology, 3, e422. doi:10.1371/journal.pbio.0030422.PubMedCrossRefGoogle Scholar
  76. Moniz, M. B. J., & Kaczmarska, I. (2009). Barcoding diatoms: Is there a good marker? Molecular Ecology Resources, 9, 65–74.PubMedCrossRefGoogle Scholar
  77. Moniz, M. B. J., & Kaczmarska, I. (2010). Barcoding of diatoms: Nuclear encoded ITS revisited. Protist, 161, 7–34.PubMedCrossRefGoogle Scholar
  78. Morales, E. A., Siver, P. A., & Trainor, F. R. (2001). Identification of diatoms (Bacillariophyceae) during ecological assessments: Comparison between light microscopy and scanning electron microscopy techniques. Proceedings of the Academy of Natural Sciences of Philadelphia, 151, 95–103.CrossRefGoogle Scholar
  79. Moritz, C., & Cicero, C. (2004). DNA barcoding: Promise and pitfalls. PLoS Biology, 2, 1529–1531.CrossRefGoogle Scholar
  80. Müller, K. (2005). SeqState – primer design and sequence statistics for phylogenetic DNA data sets. Applied Bioinformatics, 4, 65–69.PubMedCrossRefGoogle Scholar
  81. Müller, T., Philippi, N., Dandekar, T., Schultz, J., & Wolf, M. (2007). Distinguishing species. RNA, 13, 1469–1472.PubMedCrossRefGoogle Scholar
  82. Nelles, L., Fang, B. L., Volckaert, G., Vandenberghe, A., & De Wachter, R. (1984). Nucleotide sequence of a crustacean 18S ribosomal RNA gene and secondary structure of eukaryotic small subunit ribosomal RNAs. Nucleic Acid Research, 12, 8749–8768.CrossRefGoogle Scholar
  83. Newmaster, S. G., Fazekas, A., Steeves, R., & Janovec, J. (2008). Testing candidate plant barcode regions in the Myristicaceae. Molecular Ecology Resources, 8, 480–490.PubMedCrossRefGoogle Scholar
  84. Nickrent, D. L., & Sargent, M. L. (1991). An overview of the secondary structure of the V4 region of eukaryotic small-subunit ribosomal RNA. Nucleic Acid Research, 19, 227–235.CrossRefGoogle Scholar
  85. Poulíčková, A., Špačková, J., Kelly, M. G., Duchoslav, M., & Mann, D. G. (2008). Ecological variation within Sellaphora species complexes (Bacillariophyceae): Specialists or generalists? Hydrobiologia, 614, 373–386.CrossRefGoogle Scholar
  86. Powers, T. (2004). Nematode molecular diagnostics: From bands to barcodes. Annual Review of Phytopathology, 42, 367–38.PubMedCrossRefGoogle Scholar
  87. R Development Core Team. (2005). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  88. Ratnasingham, S., & Hebert, P. D. N. (2007). BOLD: The barcode of life data system. Molecular Ecology Notes, 7, 355–364.PubMedCrossRefGoogle Scholar
  89. Ravin, N. V., Galachyants, Y. P., Merdanov, A. V., Beletsky, A. V., Petrova, D. P., Sherbakova, T. A., et al. (2010). Complete sequence of the mitochondrial genome of a diatom alga Synedra acus and comparative analysis of diatom mitochondrial genomes. Current Genetics, 56, 215–223.PubMedCrossRefGoogle Scholar
  90. Robba, L., Russell, S. J., Barker, G. L., & Brodie, J. (2006). Assessing the use of the mitochondrial cox1 marker for use in DNA barcoding of red algae (Rhodophyta). American Journal of Botany, 93, 1101–1108.PubMedCrossRefGoogle Scholar
  91. Romari, K., & Vaulot, D. (2004). Composition and temporal variability of picoeukaryote communities at a coastal site of the English Channel from 18S rDNA sequences. Limnology and Oceanography, 49, 784–798.CrossRefGoogle Scholar
  92. Round, F. E., Crawford, R. M., & Mann, D. G. (1990). The diatoms – biology and morphology of the genera. Cambridge: Cambridge University Press.Google Scholar
  93. Sarno, D., Kooistra, W. H. C. F., Medlin, L. K., Percopo, I., & Zingone, A. (2005). Diversity in the genus Skeletonema (Bacillariophyceae). II: An assessment of the taxonomy of S. costatum–like species with the description of four new species. Journal of Phycology, 41, 151–176.CrossRefGoogle Scholar
  94. Saunders, G. W. (2005). Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future application. Philosophical Transactions of the Royal Society of London, Biological Sciences, 360, 1879–1888.CrossRefGoogle Scholar
  95. Saunders, G. W. (2008). A DNA barcode examination of the red algal family Dumontiaceae in Canadian waters reveals substantial cryptic species diversity. 1. The foliose Dilsea-Neodilsea complex and Weeksia. Botany, 86, 773–789.CrossRefGoogle Scholar
  96. Savin, M. C., Martin, J. L., Giewat, M., & Rooney-Varga, J. (2004). Plankton diversity in the Bay of Fundy as measured by morphological and molecular methods. Microbial Ecology, 48, 51–65.PubMedCrossRefGoogle Scholar
  97. Schloss, P. D. (2010). The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Computational Biology, 6, e1000844. doi:10.1371/journal.pcbi.1000844.PubMedCrossRefGoogle Scholar
  98. Scicluna, S. M., Tawari, B., & Clark, C. G. (2006). DNA barcoding of Blastocystis. Protist, 157, 77–85.PubMedCrossRefGoogle Scholar
  99. Seifert, K. A., Samson, R. A., de Waard, J. R., Houbraken, J., Lévesque, C. A., Moncalvo, J. M., et al. (2007). Prospects for fungus identification using COI DNA barcodes, with Penicillium as a test case. Proceedings of the National Academy of Sciences of the USA, 104, 3901–3906.PubMedCrossRefGoogle Scholar
  100. Smetacek, V. (1999). Diatoms and the carbon ocean cycle. Protist, 150, 25–32.PubMedCrossRefGoogle Scholar
  101. Sorhannus, U. (2007). A nuclear-encoded small-subunit ribosomal RNA timescale for diatom evolution. Marine Micropaleontology, 65, 1–12.CrossRefGoogle Scholar
  102. Spamer, E. E., & Theriot, E. C. (1997). “Stephanodiscus minutulus”, “S. minutus”, and similar epithets in taxonomic, ecological, and evolutionary studies of modern and fossil diatoms (Bacillariophyceae: Thalassiosiraceae)—A century and a half of uncertain taxonomy and nomenclatural hearsay. Proceedings of the Academy of Natural Sciences of Philadelphia, 148, 231–272.Google Scholar
  103. Stevenson, R. J., & Pan, Y. (1999). Assessing ecological conditions in rivers and streams with diatoms. In E. P. Stoermer & J. P. Smol (Eds.), The diatoms: Applications to the environmental and earth sciences (pp. 11–40). Cambridge: Cambridge University Press.Google Scholar
  104. Stoeckle, M. (2003). Taxonomy, DNA and the barcode of life. Bioscience, 53, 2–3.CrossRefGoogle Scholar
  105. Stoermer, E. P., & Smol, J. P. (1999). The diatoms: Applications to the environmental and earth sciences. Cambridge: Cambridge University Press.Google Scholar
  106. Summerbell, R. C., Lévesque, C. A., Seifert, K. A., Bovers, M., Fell, J. W., Diaz, M. R., et al. (2005). Microcoding: The second step in DNA barcoding. Philosophical Transactions of the Royal Society of London, Biological Sciences, 360, 1897–1903.CrossRefGoogle Scholar
  107. Swofford, D. L. (2002). PAUP*: Phylogenetic Analyses Using Parsimony (* and other methods). 4.0 beta. Sunderland: Sinauer Associates.Google Scholar
  108. Taylor, J., Bruns, T., & Lutzoni, F. (2008). ITS as the fungal barcode. http://www.allfungi.com/its-barcode.php. Accessed 30 December 2010.
  109. Teubner, K. (1997). Merkmalsvariabilität bei planktischen Diatomeen in Berlin-Brandenburger Gewässern. Nova Hedwigia, 65, 233–250.Google Scholar
  110. Utz, L. R., & Eizirik, E. (2007). Molecular phylogenies of subclass Peritrichia (Ciliophora: Oligohymenophorea) based on expanded analyses of 18S rRNA sequences. Journal of Eukaryotic Microbiology, 54, 303–305.PubMedCrossRefGoogle Scholar
  111. Vanelslander, B., Créach, V., Vanormelingen, P., Ernst, A., Chepurnov, V. A., Sahan, E., et al. (2009). Ecological differentiation between sympatric pseudocryptic species in the estuarine benthic diatom Navicula phyllepta (Bacillariophyceae). Journal of Phycology, 45, 1278–1289.CrossRefGoogle Scholar
  112. Ward, R., Zemlack, T. S., Innes, B. H., Last, P. R., & Hebert, P. D. N. (2005). DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London, Biological Sciences, 360, 1847–1857.CrossRefGoogle Scholar
  113. Wolf, M., Scheffler, W., & Nicklisch, A. (2002). Stephanodiscus neoastraea and Stephanodiscus heterostylus (Bacillariophyceae) are one and the same species. Diatom Research, 17, 445–451.Google Scholar
  114. Wu, S. G., Wang, G. T., Xi, B. W., Gao, D., & Nie, P. (2008). Molecular characteristics of Camallanus spp. (Spirurida: Camallanidae) in fishes from China based on its rDNA sequences. Journal of Parasitology, 94, 731–736.PubMedGoogle Scholar
  115. Xia, X. H., Xie, Z., & Kjer, K. M. (2003). 18S ribosomal RNA and tetrapod phylogeny. Systematic Biology, 52, 283–295.PubMedCrossRefGoogle Scholar
  116. Zechman, F. W., Zimmer, E. A., & Theriot, E. C. (1994). Use of ribosomal DNA internal transcribed spacers for phylogenetic studies in diatoms. Journal of Phycology, 30, 507–512.CrossRefGoogle Scholar
  117. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31, 3406–3415.PubMedCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2011

Authors and Affiliations

  • Jonas Zimmermann
    • 1
    • 2
  • Regine Jahn
    • 1
  • Birgit Gemeinholzer
    • 2
  1. 1.Botanic Garden and Botanical Museum Berlin-DahlemFreie Universität BerlinBerlinGermany
  2. 2.Justus Liebig UniversityGiessenGermany

Personalised recommendations