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Research Article

Morphological variability and genetic marker stability of 16 monoclonal pennate diatom strains under medium-term culture

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Pages 307-328 | Received 28 Mar 2022, Accepted 26 Sep 2022, Published online: 02 Dec 2022

References

  • Abarca N., Jahn R., Zimmermann J. & Enke N. 2014. Does the cosmopolitan diatom Gomphonema parvulum (Kützing) Kützing have a biogeography? PLoS One 9: e86885. doi:10.1371/journal.pone.0086885.
  • Abarca N., Zimmermann J., Kusber W.-H., Mora D., Van A. T., Skibbe O. & Jahn R. 2020. Defining the core group of the genus Gomphonema Ehrenberg with molecular and morphological methods. Botany Letters. 167: 114–159. doi:10.1080/23818107.2019.1694980.
  • Ashworth M.P., Nakov T. & Theriot E.C. 2013. Revisiting Ross and Sims (1971): toward a molecular phylogeny of the Biddulphiaceae and Eupodiscaceae (Bacillariophyceae). Journal of Phycology 49: 1207–1222 doi:10.1111/jpy.12131.
  • Assmy P., Henjes J., Smetacek V. & Montresor M. 2006. Auxospore formation by the silica-sinking, oceanic diatom Fragilariopsis kerguelensis (Bacillariophyceae). Journal of Phycology 42: 1002–1006. doi:10.1111/j.1529-8817.2006.00260.x.
  • Barreto Filho M.M., Walker M., Ashworth M.P. & Morris J.J. 2021. Structure and long-term stability of the microbiome in diverse diatom cultures. American Society for Microbiology ASM 9: e00269-21. doi:10.1128/Spectrum.00269-21.
  • 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. doi:10.1046/j.1529-8817.2004.03037.
  • Beszteri B., Acs E., Makk J., Kovacs G., Marialigeti K. & Kiss K.T. 2001. Phylogeny of six naviculoid diatoms based on 18S rDNA sequence. International Journal of Systematic and Evolutionary Microbiology 51: 1581–1586.
  • Bruder K., Sato S. & Medlin L. 2008. Morphological and molecular investigations of naviculoid diatoms IV. Pinnularia vs. Caloneis. Diatom 24: 8–24.
  • Cox E.J.1993. Freshwater diatom ecology: developing an experimental approach as an aid to interpreting field data. Hydrobiologia 269: 447–452. doi:10.1007/BF00028042.
  • Cox E.J. 2015. Diatoms, Diatomeae (Bacillariophyceae s.l., Bacillariophyta). In: Syllabus of plant families (13th edition) (Ed. by W. Frey), Vol. 2/1, pp. 64–103. Borntraeger Science Publishers, Stuttgart.
  • Crawford R.M. 1981. Some considerations of size reduction in diatom cell walls. In: Proceedings of the 6th symposium on recent and fossil diatoms (Ed. by R. Ross), pp. 253–262. Koeltz Scientific Books, Königstein.
  • Davidovich N.A., Davidovich O.I., Podunay Y.A., Polyakova S.L. & Gastineau R. 2019. Decontamination of Diatom Algae cultures contaminated with the Kinetoplastid Bodo saltans Ehrenberg, 1832. Moscow University Biological Science Bullentin 74: 63–68.
  • Downey K.M., Julius M.L., Theriot E.C. & Alverson A. 2021. Phylogenetic analysis places Spicaticribra within Cyclotella. Diatom Research 36: 1–7. doi:10.1080/0269249X.2021.1926332.
  • Drebes G. 1977. Cell structure, cell division, and sexual reproduction of Attheya decora West (Bacillariophyceae, Biddulphiinae). Beihefte zur Nova Hedwigia 54: 167–178.
  • Dreßler M., Werner P., Adler S., Kahlert M., Verweij G., Schwarz A., van der Wal J., Kistenich S., Hübener T., Fazzone A. & Galbiati M. 2014. Erster deutscher Ringversuch benthische Diatomeen 2011/2012. Abschlussbericht September 2014 [online]. Available from: https://www.planktonforum.eu/fileadmin/user_upload/EQAT_Phytoplankton_RV_Benthische_Diatomeen_2011_2012_Abschlussbericht.pdf.
  • Droege G., Barker K., Astrin J.J., Bartels P., Butler C., Cantrill D., Coddington J., Forest F., Gemeinholzer B., Hobern D., Mackenzie-Dodds D., Tuama É.Ó., Petersen G., Sanjur O., Schindel D. & Seberg O. 2014. The global genome biodiversity network (GGBN) data portal. Nucleic Acids Research 42 (D1): D607–D612. doi:10.1093/nar/gkt928.
  • Edgar R.C. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460–2461. doi:10.1093/bioinformatics/btq461.
  • Edgar S.M. & Theriot E.C. 2004. Phylogeny of Aulacoseira (Bacillariophyta) based on molecules and morphology. Journal of Phycology 40: 772–788. doi:10.1111/j.1529-8817.2004.03126.x.
  • Ehrenberg C.G. 1838. Die infusionsthierchen als voll-kommene Organismen: ein Blick in das tiefere organische Leben der Natur. Voss, Leipzig. 548 p.
  • Estes A. & Dute R.R. 1994. Valve abnormalities in diatom clones maintained in long-term culture. Diatom Research 9: 249–258. doi:10.1080/0269249X.1994.9705305.
  • Falasco E., Bona F., Ginepro M., Hlúbiková D., Hoffmann L. & Ector L. 2009. Morphological abnormalities of diatom silica walls in relation to heavy metal contamination and artificial growth conditions. Water SA 35: 595–606.
  • Falasco E., Bona F., Risso A.M. & Piano E. 2021. Hydrological intermittency drives diversity decline and functional homogenization in benthic diatom communities. Science of the Total Environment 762: 143090. doi:10.1016/j.scitotenv.2020.143090.
  • Gaonkar C.C., Piredda R., Minucci C., Mann D.G., Montresor M., Sarno D. & Kooistra W. 2018. Annotated 18S and 28S rDNA reference sequences of taxa in the planktonic diatom family Chaetocerotaceae. PLoS ONE 13: e0208929. doi:10.1371/journal.pone.0208929.
  • Geissler U. 1970a. Die Variabilität der Schalenmerkmale bei den Diatomeen. Nova Hedwigia 19: 623–773.
  • Geissler U. 1970b. Die Schalenmerkmale der Diatomeen. Ursachen ihrer Variabilität und Bedeutung für die Taxonomie. Beihefte zur Nova Hedwigia 31: 511–535.
  • Genkal S.I. 2004. Morphological variability and taxonomy of Diatoma tenue Ag. (Bacillariophyta). International Journal on Algae 6: 319–330. doi:10.1615/InterJAlgae.v6.i4.20.
  • Goujon M., McWilliam H., Li W., Valentin F., Squizzato S., Paern J. & Lopez R. 2010. A new bioinformatics analysis tools framework at EMBL–EBI. Nucleic Acids Research 38: W695–W699. doi:10.1093/nar/gkq313.
  • Gruenstaeudl M. 2020. Annonex2embl: automatic preparation of annotated DNA sequences for bulk submissions to ENA. Bioinformatics 36:3841–3848. doi:10.1093/bioinformatics/btaa209.
  • Håkansson H. & Chepurnov V. 1999. A study of variation in valve morphology of the diatom Cyclotella meneghiniana in monoclonal cultures: effect of auxospore formation and different salinity conditions. Diatom Research 14: 251–272.
  • Hofmann G., Lange-bertalot H. & Werum M. 2013. Diatomeen im Süßwasser -Benthos von Mitteleuropa. Bestimmungsflora Kieselalgen für die ökologische Praxis. Über 700 der häufigsten Arten und ihre Ökologie. Koeltz Scientific Books, Königstein.
  • Jahn R. 1986. A study of Gomphonema augur Ehrenberg: the structure of the frustule and its variability in clones and populations. In: Proceedings of the 8th international diatom symposium (Ed. by M. Ricard), pp. 191–204. Koeltz, Königstein.
  • Jahn R., Abarca N., Al-Handal A., Kusber W.-H., Zimmermann J. & Skibbe O. 2021. Integrative taxonomic description of the marine species Cocconeis crawfordii (Bacillaiophyceae) based on unialgal strains. Nova Hedwigia, Beiheft 151: 85–105.
  • Jahn R., Abarca N., Gemeinholzer B., Mora D., Skibbe O., Kulikovskiy M., Gusev E., Kusber W.-H. & Zimmermann J. 2017a. Planothidium lanceolatum and Planothidium frequentissimum reinvestigated with molecular methods and morphology: four new species and the taxonomic importance of the sinus and cavum. Diatom Research 32: 75–107. doi:10.1080/0269249X.2017.1312548.
  • Jahn R., Abarca N., Kusber W.-H., Skibbe O., Zimmermann J. & Mora D. 2020. Integrative taxonomic description of two new species of the Cocconeis placentula group (Bacillariophyceae) from Korea based on unialgal strains. Algae 35: 303–324. doi:10.4490/algae.2020.35.8.1.
  • Jahn R., Kusber W.-H. & Cocquyt C. 2017b. Differentiating Iconella from Surirella (Bacillariophyceae): typifying four Ehrenberg names and a preliminary checklist of the African taxa. Phytokeys 82:73–112. doi:10.3897/phytokeys.82.13542.
  • Kaczmarska I. & Ehrman J.M. 2015. Auxosporulation in Paralia guyana MacGillivary (Bacillariophyta) and possible new insights into the habit of the earliest diatoms. PLoS One 10: e0141150. doi:10.1371/journal.pone.0141150.
  • Kaczmarska I. & Ehrman J.M. 2021. Enlarge or die! An auxospore perspective on diatom diversification. Organisms Diversity & Evolution 21. doi:10.1007/s13127-020-00476-7.
  • Kaczmarska I., Pouličkova A., Sato S., Edlund M. B., Idei M., Watanabe T. & Mann D.G. 2013. Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages. Diatom Research 28:263–294. doi:10.1080/0269249X.2013.791344.
  • Kim S.Y., Witkowski A., Park J.G., Gastineau R., Ashworth M., Kim B.S., Mann D.G., Li C.L., Igersheim A., Plocinski T., Yoo Y.D., Chung S.O. & Theriot E.C. 2020. The taxonomy and diversity of Proschinia (Bacillariophyta), a common but enigmatic genus from marine coasts. Journal of Phycology 56. doi:10.1111/jpy.12998.
  • Krammer K. 2000. The genus Pinnularia. In: Diatoms of Europe, diatoms of European Inland waters and comparable habitats (Ed. by H. Lange-Bertalot), Vol. 1, 703 pp. A.R.G. Gantner Verlag K.G., Ruggell.
  • Krammer K. & Lange-Bertalot H. 1986. Bacillariophyceae. 1. Teil: Naviculaceae. In: Süßwasserflora von Mitteleuropa (Ed. by H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer), pp. 2/1, 876. Gustav Fischer Verlag, Stuttgart.
  • Krammer K. & Lange-Bertalot H. 1991. Bacillariophyceae. 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In: Süßwasserflora von Mitteleuropa (Ed. by H. Ettl, J. Gerloff, H. Heynig & D. Mollenhauer), Vol. 2/3, 576 pp. Gustav Fischer Verlag, Stuttgart.
  • Kulikovskiy M., Gusev E., Andreeva S. & Annenkova N. 2014. Phylogenetic position of the diatom genus Geissleria Lange-Bertalot & Metzeltin and description of two new species from Siberian mountain lakes. Phytotaxa 177: 249–260. doi:10.11646/phytotaxa.177.5.1.
  • Lange-Bertalot H., Hofmann G., Werum M. & Cantonati M. 2017. Freshwater benthic diatoms of Central Europe: over 800 common species used in ecological assessment. Koeltz Botanical Books, Schmitten-Oberreifenberg.
  • Li Y., Nagumo T & Xu K. 2021. Morphology and molecular phylogeny of Amphora baotuensis sp. nov., a new freshwater benthic diatom from a karst spring in China. Diatom Research 37: 145–153. doi:10.1080/0269249X.2022.2063390.
  • Mann, D.G. 1989. On auxospore formation in Caloneis and the nature of Amphiraphia (Bacillariophyta). Plant Systematics and Evolution 163: 43–52. doi:10.1007/BF00936152.
  • Mann D.G. 1999. The species concept in diatoms (Phycological reviews 18). Phycologia 38: 437–495. doi:10.2216/i0031-8884-38-6-437.1.
  • Mann D.G. 2011. Size and sex. In: The diatom world (Ed. by J. Seckbach & J.P. Kociolek), pp. 147–166. Springer, Dordrecht.
  • Mann D.G. & Chepurnov V.A. 2004. What have the Romans ever done for us? The past and future contribution of culture studies to diatom systematics. Nova Hedwigia 79: 237–291. doi:10.1127/0029-5035/2004/0079-0237.
  • Mann D.G., Simpson G.E., Sluiman H.J. & Möller M. 2001. Rbcl gene tree of diatoms: a second large data-set for phylogenetic reconstruction. Phycologia 40: Supplement: 1–2.
  • Manoylov K.M. 2009. Intra- and interspecific competition for nutrients and light in diatom cultures. Journal of Freshwater Ecology 24: 145–157. doi:10.1080/02705060.2009.9664275.
  • Medlin L.K., Lange M. & Nöthig E.M. 2000. Genetic diversity in the marine phytoplankton: a review and a consideration of Antarctic phytoplankton. Antarctic Science 12: 325–333.doi:10.1017/S0954102000000389.
  • Mora D., Abarca N., Proft S., Grau J.H., Enke N., Carmona J., Skibbe O., Jahn R. & Zimmermann J. 2019. Morphology and metabarcoding: a test with stream diatoms from Mexico highlights the complementarity of identification methods. Freshwater Science 38: 448–464. doi:10.1086/704827.
  • Mora D., Stancheva R. & Jahn R. 2022. Cocconeis czarneckii sp. nov. (Bacillariophyta): a new diatom species from Lake Okoboji (Iowa, USA), based on the strain UTEX FD23. Phycologia 61: 60–74. doi:10.1080/00318884.2021.2003684.
  • Müller J., Müller K., Neinhuis C. & Quandt D. 2005. PhyDE-phylogenetic data editor. Version 0.9971: Available from: http://www.phyde.de.
  • Nakov T., Guillory W., Julius M.L., Theriot E.C. & Alverson A. 2015. Towards a phylogenetic classification of species belonging to the diatom genus Cyclotella (Bacillariophyceae): transfer of the species formerly placed in Puncticulata, Handmannia, Pliocaenicus and Cyclotella to the genus Lindavia. Phytotaxa 217:249–264. doi:10.11646/phytotaxa.217.3.2.
  • Petrova D.P., Bedoshvili Y. D., Zakharova Y.R., Volokitina N. A., Likhoshway Y.V. & Grachev M. A. 2020. Changes in valve morphology of two pennate diatom species during long-term culture. Acta Biologica Sibirica 6: 669–678. doi:10.3897/abs.6.e57888.
  • Pinseel E., Kulichová J., Scharfen V., Urbánková P., Van de Vijver B. & Vyverman W. 2019. Extensive cryptic diversity in the terrestrial diatom Pinnularia borealis (Bacillariophyceae). Protist 170: 121–140. doi:10.1016/j.protis.2018.10.001.
  • Pinseel E., Vanormelingen P., Hamilton P.B., Vyverman W., Van de Vijver B. & Kopalova K. 2017. Molecular and morphological characterization of the Achnanthidium minutissimum complex (Bacillariophyta) in Petuniabukta (Spitsbergen, High Arctic) including the description of A. digitatum sp. nov. European Journal of Phycology 52: 264–280. doi:10.1080/09670262.2017.1283540.
  • Rimet F., Chaumeil P., Keck F., Kermarrec L., Vasselon V., Kahlert M., Franc A. & Bouchez A. 2016. R-Syst::diatom: an open-access and curated barcode database for diatoms and freshwater monitoring. Database. 1–21. doi:10.1093/database/baw016.
  • Rose D.T. & 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. doi:10.1127/1863-9135/2013/0406.
  • Rose D.T. & Cox E.J. 2014. What constitutes Gomphonema parvulum? Long-term culture studies show that some varieties of G. parvulum belong to other Gomphonema species. Plant Ecology and Evolution 147: 366–373. doi:10.5091/plecevo.2014.1059.
  • Round F.E. 1992. A re-investigation of some fragilarioid diatoms in the Provasoli/Guillard culture collection. Diatom Research 7: 303–311. doi:10.1080/0269249X.1992.9705222.
  • Round F.E. 1993. A Synedra (Bacillariophyta) clone after several years in culture. Nova Hedwigia Beiheft 106: 353–359.
  • Round F.E., Crawford R.M. & Mann D.G. 1990. Diatoms: biology and morphology of the genera. Cambridge University Press, Cambridge. 747 pp.
  • Ruck E.C., Nakov T., Alverson A.J. & Theriot E.C. 2016. Phylogeny, ecology, morphological evolution, and reclassification of the diatom orders Surirellales and Rhopalodiales. Molecular Phylogenetics and Evolution 103: 155–171. doi:10.1016/j.ympev.2016.07.023.
  • Sabbe K., Chepurnov V.A., Mann D.G. & Vyverman W. 2004. Sexual behaviour, auxosporulation and chloroplast dynamics in a marine Amphora (Bacillariophyceae) studied in culture. Botanica Marina 47: 53–63. doi:10.1515/BOT.2004.006.
  • Sato S., Nagumot T. & Tanaka J. 2004. Auxospore formation and the morphology of the initial cell of the marine araphid diatom Gephyria media (Bacillariophyceae). Journal of Phycology 40: 648–691. doi:10.1111/j.1529-8817.2004.03164.x.
  • Sato S., Mann D.G., Nagumo T., Tanaka J., Tadano T. & Medlin L.K. 2008. Auxospore fine structure and variation in modes of cell size changes in Grammatophora marina (Bacillariophyta). Phycologia 47: 12–27.
  • Saunders G.W. 2005. Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philosophical Transactions of the Royal Society of London B: Biological Sciences 360: 1879–1888.
  • Schmid A.M.M. 1979. Influence of environmental factors on the development of the valve in diatoms. Protoplasma 99: 99–115.
  • Schmid A.M.M. 2009. Induction of resting-spores in the pennate diatom Navicula (Craticula) cuspidata by uncoupling of the cell and plastid cycles. Nova Hedwigia, Beiheft 135: 85–101.
  • Schultz K., Hübener T., Jacques O., Springer A., Frank M & Dreßler M. 2022. DNA barcoding reveals a new species of Stephanodiscus Ehrenberg. Diatom Research. doi:10.1080/0269249X.2022.2078427.
  • Souffreau C., Verbruggen H., Wolfe A.P., Vanormelingen P., Siver P.A., Cox E.J., Mann D.G., Van de Vijver B., Sabbe K. & Vyverman W. 2011. A time-calibrated multi-gene phylogeny of the diatom genus Pinnularia. Molecular Phylogenetics and Evolution 61: 866–879. doi:10.1016/j.ympev.2011.08.031.
  • Stachura-Suchoples K., Enke N., Schlie C., Schaub I., Karsten U. & Jahn R. 2016. Contribution towards a morphological and molecular taxonomic reference library of benthic marine diatoms from two Arctic fjords on Svalbard (Norway). Polar Biology 39: 1933–1956. doi:10.1007/s00300-015-1683-2.
  • Su Y., Lundholm N. & Ellegaard M. 2017. Long-term cultivation of the diatom Coscinodiscus granii at different light spectra: effects on frustule morphology. Journal of Applied Phycology 29: 1775–1779. doi:10.1007/s10811-017-1101-y.
  • Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. doi:10.1093/molbev/mst197.
  • Trobajo R., Clavero E., Chepurnov V.A., Sabbe K., Mann D.G., Ishihara S. & Cox E.J. 2009. Morphological, genetic and mating diversity within the widespread bioindicator Nitzschia palea (Bacillariophyceae). Phycologia 48: 443–459. doi:10.2216/08-69.1.
  • Windler M., Bova D., Kryvenda A., Straile D., Gruber A.G. & Kroth P. 2014. Influence of bacteria on cell size development and morphology of cultivated diatoms. Phycological Research 62: 269–281. doi:10.1111/pre.12059.
  • Witkowski A., Ashworth M., Li C., Sagna I., Yatte D., Górecka E., Franco A.O.R., Kusber W.-H., Klein G., Lange-Bertalot H., Przemysław D., Theriot E.C. & Manning S.R. 2020. Exploring diversity, taxonomy and phylogeny of diatoms (Bacillariophyta) from marine habitats. Novel taxa with internal costae. Protist 171: 125713. doi:10.1016/j.protis.2020.125713.
  • Zimmermann J., Abarca N., Enke N., Skibbe O., Kusber W.-H. & Jahn R. 2014. Taxonomic reference libraries for environmental barcoding: a best practice example from diatom research, PLoS ONE 9: e108793. doi:10.1371/journal.pone.0108793.
  • Zimmermann J., Jahn R. & Gemeinholzer B. 2011. Barcoding diatoms: evaluation of the V4 subregion on the 18S rRNA gene, including new primers and protocols. Organisms Diversity and Evolution 11: 173–192. doi:10.1007/s13127-011-0050-6.

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