Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-25T16:11:06.528Z Has data issue: false hasContentIssue false
  • English
  • Français

Exploring cryptic diversity in publicly available strains of the model diatom Thalassiosira pseudonana (Bacillariophyceae)

Published online by Cambridge University Press:  17 April 2015

Cecilia Rad-Menéndez ,
Michele Stanley ,
David H. Green ,
Eileen J. Cox  and
John G. Day
Cecilia Rad-Menéndez*
Affiliation:
Culture Collection of Algae and Protozoa, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK Microbial & Molecular Biology Department, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK
Michele Stanley
Affiliation:
Microbial & Molecular Biology Department, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK
David H. Green
Affiliation:
Microbial & Molecular Biology Department, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK
Eileen J. Cox
Affiliation:
Department of Botany, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
John G. Day
Affiliation:
Culture Collection of Algae and Protozoa, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK Microbial & Molecular Biology Department, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK
*
Correspondence should be addressed to: C. Rad-Menéndez, Culture Collection of Algae and Protozoa, Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll PA37 1QA, UK email: crm@sams.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

The model diatom Thalassiosira pseudonana is believed to be a single species with a global distribution, but it has not been confirmed previously whether isolates from different environmental and geographic origins are genotypically and phenotypically identical. In the present study, a polyphasic approach was employed to characterize nine clonal isolates, plus an additional replicate of one of the isolates, of the diatom T. pseudonana from culture collections to investigate whether there was any cryptic speciation in the publicly available strains of this species. Morphological analysis using scanning electron microscopy concluded that the strains were indistinguishable. Furthermore, conventional DNA barcoding genes (SSU rDNA, ITS1 and ITS2 rDNA and rbcL), revealed no nucleotide variation among the strains tested. On employing a whole genome fingerprinting technique, Amplified Fragment Length Polymorphism (AFLP), three clusters were revealed, although the level of variation between the clusters was surprisingly low. These findings indicate a low level of diversity among these cultured T. pseudonana strains, despite their wide spatial and temporal distribution and the salinity range of their original habitats. Based on the limited number of available strains, this suggests that T. pseudonana is a highly conserved diatom that nevertheless has an ability to tolerate wide ranges of salinity and populate varied geographic locations.

Keywords

Amplified Fragment Length Polymorphism (AFLP)DNA barcodingfingerprintingThalassiosira pseudonanaCyclotella nana
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 6 , September 2015 , pp. 1081 - 1090
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ake-Castillo, J.A., Hernandez-Becerril, D.U. and Meave Del Castillo, M.E. (1999) Species of the genus Thalassiosira (Bacillariophyceae) from the Gulf of Tehuantepec, Mexico. Botanica Marina 42, 487–503.CrossRefGoogle Scholar
Alverson, A.J., Beszteri, B., Julius, M. and Theriot, E. (2011) The model marine diatom Thalassiosira pseudonana likely descended from a freshwater ancestor in the genus Cyclotella. BMC Evolutionary Biology 11, 125.CrossRefGoogle ScholarPubMed
Alverson, A.J., Jansen, R.K. and Theriot, E.C. (2007) Bridging the rubicon: phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Molecular Phylogenetics and Evolution 45, 193–210.CrossRefGoogle ScholarPubMed
Amato, A., Kooistra, W.H.C.F., Levialdi Ghiron, J.H., Mann, D.G., Pröschold, T. and Montresor, M. (2007) Reproductive isolation among sympatric cryptic species in marine diatoms. Protist 158, 193–207.CrossRefGoogle ScholarPubMed
Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H., Zhou, S., Allen, A.E., Apt, K.E., Bechner, M., Brzezinski, M.A., Chaal, B.K., Chiovitti, A., Davis, A.K., Demarest, M.S., Detter, J.C., Glavina, T., Goodstein, D., Hadi, M.Z., Hellsten, U., Hildebrand, M., Jenkins, B.D., Jurka, J., Kapitonov, V.V., Kröger, N., Lau, W.W.Y., Lane, T.W., Larimer, F.W., Lippmeier, J.C., Lucas, S., Medina, M., Montsant, A., Obornik, M., Parker, M.S., Palenik, B., Pazour, G.J., Richardson, P.M., Rynearson, T.A., Valentin, K., Vardi, A., Wilkerson, F.P. and Rokhsar, D.S. (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism. Science 306, 79–86.CrossRefGoogle ScholarPubMed
Baillie, B.K., Belda-Baillie, C.A. and Maruyama, T. (2000) Conspecificity and Indo-Pacific distribution of Symbiodinium genotypes (Dinophyceae) from giant clams. Journal of Phycology 36, 1153–1161.CrossRefGoogle Scholar
Barker, G.L.A., Green, J.C., Hayes, P.K. and Medlin, L.K. (1994) Preliminary results using the RAPD analysis to screen bloom populations of Emiliana huxleyi (Haptophyta). Sarsia 79, 301–306.CrossRefGoogle Scholar
Belcher, J.H. and Swale, E.M.F. (1977) Species of Thalassiosira diatoms (Bacillariophyceae) in the plankton of English rivers. British Phycological Journal 12, 291–296.CrossRefGoogle Scholar
Beszteri, B., John, U. and 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 polymorphisms. European Journal of Phycology 42, 47–60.CrossRefGoogle Scholar
Casteleyn, G., Chepurnov, V.A., Leliaert, F., Mann, D.G., Bates, S.S., Lundholm, N., Rhodes, L., Sabbe, K. and Vyverman, W. (2008) Pseudo-nitzschia pungens (Bacillariophyceae): a cosmopolitan diatom species? Harmful Algae 7, 241–257.CrossRefGoogle Scholar
Coleman, A.W., Suarez, A. and Goff, L.J. (1994) Molecular delineation of species and syngens in Volvocacean green algae (Chlorophyta). Journal of Phycology 30, 80–90.CrossRefGoogle Scholar
Darienko, T., Gustavs, L., Mudimu, O., Rad-Menendez, C., Schumann, R., Karsten, U., Friedl, T. and Pröschold, T. (2010) Chloroidium, a common terrestrial coccoid green alga previously assigned to Chlorella (Trebouxiophyceae, Chlorophyta). European Journal of Phycology 45, 79–95.CrossRefGoogle Scholar
Davey, J.W., Hohenlohe, P.A., Etter, P.D., Boone, J.Q., Catchen, J.M. and Blaxter, M.L. (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics 12, 499–510.CrossRefGoogle ScholarPubMed
De Martino, A., Meichenin, A., Shi, J., Pan, K. and Bowler, C. (2007) Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions. Journal of Phycology 43, 992–1009.CrossRefGoogle Scholar
Evans, K.M., Chepurnov, V.A., Sluiman, H.J., Thomas, S.J., Spears, B.M. and Mann, D.G. (2009) Highly differentiated populations of the freshwater diatom Sellaphora capitata suggest limited dispersal and opportunities for allopatric speciation. Protist 160, 386–396.CrossRefGoogle ScholarPubMed
Evans, K.M., Wortley, A.H. and 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.CrossRefGoogle ScholarPubMed
Evans, K.M., Wortley, A.H., Simpson, G.E., Chepurnov, V.A. and 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 ScholarPubMed
Guillard, R.R.L. (1975) Culture of phytoplankton for feeding marine invertebrates. In Smith, W.L. and Chanley, M. H. (eds) Culture of marine invertebrate animals. New York: Plenum Publishing, pp. 29–60.CrossRefGoogle Scholar
Hamsher, S.E., Evans, K.M., Mann, D.G., Poulícková, A. and Saunders, G.W. (2011) Barcoding diatoms: exploring alternatives to COI-5P. Protist 162, 405–422.CrossRefGoogle ScholarPubMed
Hasle, G.R. (1978) Some freshwater and brackish water species of the diatom genus Thalassiosira Cleve. Phycologia 17, 263–292.CrossRefGoogle Scholar
Hasle, G.R. and Heimdal, B.R. (1970) Some species of the centric diatom genus Thalassiosira studied in the light and electron microscopes. Beihefte zur Nova Hedwigia 31, 543–581.CrossRefGoogle Scholar
Hildebrand, M., Frigeri, L. and Davis, A.K. (2007) Synchronized growth of Thalassiosira pseudonana (Bacillariophyceae) provides novel insights into cell wall synthesis processes in relation to the cell cycle. Journal of Phycology 43, 730–740.CrossRefGoogle Scholar
John, U., Groben, R., Beszteri, B. and Medlin, L. (2004) Utility of amplified fragment length polymorphisms (AFLP) to analyse genetic structures within the Alexandrium tamarense species complex. Protist 155, 169–179.CrossRefGoogle ScholarPubMed
Jones, H.M., Simpson, G.E., Stickle, A.J. and Mann, D.G. (2005) Life history and systematics of Petroneis (Bacillariophyta) with special reference to British waters. European Journal of Phycology 40, 61–87.CrossRefGoogle Scholar
Kooistra, W.H.C.F., Sarno, D., Balzano, S., Gu, H., Andersen, R.A. and Zingone, A. (2008) Global diversity and biogeography of Skeletonema species (Bacillariophyta). Protist 159, 177–193.CrossRefGoogle ScholarPubMed
Lowe, R.L. and Busch, D.E. (1975) Morphological observations on two species of the diatom genus Thalassiosira from fresh-water habitats in Ohio. Transactions of the American Microscopical Society 94, 118–123.CrossRefGoogle Scholar
Lundholm, N., Daugbjerg, N. and Moestrup, Q. (2002) Phylogeny of the Bacillariaceae with emphasis on the genus Pseudo-nitzschia (Bacillariophyceae) based on partial LSU r DNA. European Journal of Phycology 37, 115–134.CrossRefGoogle Scholar
Luo, W., Pflugmacher, S., Pröschold, T., Walz, N. and Krienitz, L. (2006) Genotype versus phenotype variability in Chlorella and Micractinium (Chlorophyta, Trebouxiophyceae). Protist 157, 315–333.CrossRefGoogle ScholarPubMed
Mann, D.G., Chepurnov, V.A. and Idei, M. (2003) Mating system, sexual reproduction and auxosporulation in the anomalous raphid diatom Eunotia (Bacillariophyta). Journal of Phycology 39, 1067–1084.CrossRefGoogle Scholar
Mann, D.G., Thomas, S.J. and Evans, K.M. (2008) Revision of the diatom genus Sellaphora: a first account of the larger species in the British Isles. Fottea 8, 15–78.CrossRefGoogle Scholar
Mannschreck, K., Klemp, D., Kley, D., Friedrich, R., Kühlwein, J., Wickert, B., Habram, M., Matuska, P. and Slemr, F. (2002) Evaluation of an emission inventory by comparison of modeled and measured emission ratios of individual HCs, CO and NOx. Atmospheric Environment 36, S81–S94.CrossRefGoogle Scholar
Marin, B., Palm, A., Klingberg, M. and Melkonian, M. (2003) Phylogeny and taxonomic revision of plastid-containing euglenophytes based on SSU rDNA sequence comparison and synapomorphic signatures in the SSU rRNA secondary structure. Protist 154, 99–145.CrossRefGoogle ScholarPubMed
Meudt, H.M. and Clarke, A.C. (2007) Almost forgotten or latest practice? AFLP applications, analyses, and advances. Trends in Plant Science 12, 106–117.CrossRefGoogle ScholarPubMed
Moniz, M.B.J. and Kaczmarska, I. (2009) Barcoding diatoms: is there a good marker? Molecular Ecology Resources 9, 65–74.CrossRefGoogle Scholar
Moniz, M.B.J. and Kaczmarska, I. (2010) Barcoding of diatoms: nuclear encoded ITS revisited. Protist 161, 7–34.CrossRefGoogle ScholarPubMed
Müller, J., Friedl, T., Hepperle, D., Lorenz, M. and Day, J.G. (2005) Distinction between multiple isolates of Chlorella vulgaris (Chlorophyta, Trebouxiophyceae) and testing for conspecificity using amplified fragment length polymorphism and ITS rDNA sequences. Journal of Phycology 41, 1236–1247.CrossRefGoogle Scholar
Nei, M. and Li, W.H. (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences USA 76, 5269–5273.CrossRefGoogle ScholarPubMed
Posada, D. and Buckley, T.R. (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Systematic Biology 53, 793–808.CrossRefGoogle ScholarPubMed
Posada, D. and Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Pröschold, T., Marin, B., Schlosser, U.G. and Melkonian, M. (2001) Molecular phylogeny and taxonomic revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas gobi, and description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152, 265–300.CrossRefGoogle ScholarPubMed
Rose, D.T. and Cox, E.J. (2013) Some diatom species do not show a gradual decrease in cell size as they reproduce. Fundamental and Applied Limnology 182, 117–122.CrossRefGoogle Scholar
Round, F.E., Crawford, R.M. and Mann, D.G. (1990) The diatoms: biology & morphology of the genera. Cambridge: Cambridge University Press.Google Scholar
Rynearson, T.A. and Armbrust, E.V. (2000) DNA fingerprinting reveals extensive genetic diversity in a field population of the centric diatom Ditylum brightwellii. Limnology and Oceanography 45, 1329–1340.CrossRefGoogle Scholar
Sarno, D., Kooistra, W.H.C.F., Medlin, L.K., Percopo, I. and 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
Saunders, G.W. (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future application. Philosophical Transactions of the Royal Society B 360, 1879–1888.CrossRefGoogle Scholar
Stern, R.F., Andersen, R.A., Jameson, I., Küpper, F.C., Coffroth, M.A., Vaulot, D., Le Gall, F., Véron, B., Brand, J.J., Skelton, H., Kasai, F., Lilly, E.L. and Keeling, P.J. (2012) Evaluating the Ribosomal Internal Transcribed Spacer (ITS) as a Candidate Dinoflagellate Barcode Marker. PLoS ONE 7(8): e42780. doi: 10.1371/journal.pone.0042780.CrossRefGoogle ScholarPubMed
Swofford, D.L. (2002) PAUP* phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sunderland, MA: Sinauer.Google Scholar
Tamura, K. and Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Tonon, T., Harvey, D., Qing, R., Li, Y., Larson, T.R. and Graham, I.A. (2004) Identification of a fatty acid D11-desaturase from the microalga Thalassiosira pseudonana. FEBS Letters 563, 28–34.CrossRefGoogle ScholarPubMed
Veselá, J., Neustupa, J., Pichrtová, M. and Poulícková, A. (2009) Morphometric study of Navicula morphospecies (Bacillariophyta) with respect to diatom life cycle. Fottea 9, 307–316.CrossRefGoogle Scholar
Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van De Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. and Zabeau, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleid Acids Research 23, 4407–4414.CrossRefGoogle ScholarPubMed
Warren, A., Day, J.G. and Brown, S. (1997) Cultivation of protozoa and algae. In Hurst, C.J., Knudsen, G.R., McInerney, M.J., Stezenbach, L.D. and Walter, M.V. (eds) Manual of environmental microbiology. Washington, DC: ASM Press, pp. 61–71.Google Scholar
Werner, R., Olschewski, J. and Mergenhagen, D. (2001) Identification and cloning of amplified fragment length polymorphism markers to the mating type locus of Chlamydomonas reinhardtii (Chlorophyta). Journal of Phycology 37, 427–432.CrossRefGoogle Scholar
Williams, J.G.K., Kubelik, A.R., Livak, K.J., Rafalski, J.A. and Tingey, S.V. (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleid Acids Research 18, 6531–6535.CrossRefGoogle ScholarPubMed
Supplementary material: File

Rad-Menéndez supplementary material

Appendix 1-2

Download Rad-Menéndez supplementary material(File)
File 42.6 KB