Plant Ecology and Evolution 152(2): 219-247, doi: 10.5091/plecevo.2019.1603
Gomphonella olivacea (Bacillariophyceae) – a new phylogenetic position for a well-known taxon, its typification, new species and combinations
expand article infoRegine Jahn‡, Wolf-Henning Kusber§, Oliver Skibbe§, Jonas Zimmermann§, Anh Tu Van§, Krisztina Buczkó|, Nélida Abarca§
‡ Botanischer Garten und Botanisches Museum Berlin‒Dahlem, Freie Universität Berlin, Berlin, Germany§ Botanischer Garten und Botanisches Museum Berlin, Freie Universität Berlin, Königin-Luise-Str. 6-8, 14195 Berlin, Germany| Department of Botany, Hungarian Natural History Museum, Könyves Kálmán krt. 40, 1087, Budapest and MTA Centre for Ecological Research, Danube Research Institute, Karolina St 29, 1113 Budapest, Hungary

Corresponding author: Regine Jahn ( r.jahn@bgbm.org )

© Regine Jahn, Wolf-Henning Kusber, Oliver Skibbe, Jonas Zimmermann, Anh Tu Van, Krisztina Buczkó, Nélida Abarca.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Jahn R, Kusber W-H, Skibbe O, Zimmermann J, Van AT, Buczkó K, Abarca N (2019) Gomphonella olivacea (Bacillariophyceae) – a new phylogenetic position for a well-known taxon, its typification, new species and combinations. Plant Ecology and Evolution 152(2): 219-247. https://doi.org/10.5091/plecevo.2019.1603
Open Access
Abstract

Background and aims – Within the project “German Barcode of Life – Diatoms” common diatoms of German waters were routinely isolated and cultivated. In order to understand the taxonomy and phylogeny of the genus Gomphonema, one of the most common taxa of Central Europe, known currently either under the name Gomphonema olivaceum in Europe or Gomphoneis olivacea in America, was studied.

Methods – Twenty unialgal strains were established from five different water bodies in Germany and one from Lake Balaton, Hungary, which supplied molecular data (18S V4 and rbcL) besides morphometric and ultrastructural data. In addition, on eight populations from different water bodies including the type from Denmark, morphometric and micromorphological studies by light and scanning electron microscopy were performed.

Key results – Molecular and micromorphological data show that the target taxon neither belongs to Gomphonema Ehrenb. nor to Gomphoneis Cleve. By reinstating the genus name Gomphonella Rabenh., the nomenclatural and taxonomic enigma of this taxon is solved, and with the presentation of the type by Hornemann the authorship of the epithet is clarified. Molecular data for the unialgal strains and several environmental clones show that there is more diversity in the Gomphonella olivacea clade than can be identified morphologically. In addition, the establishment of the new species Gomphonella coxiae and Gomphonella acsiae is supported. The molecular data classified Gomphonella species as belonging to the Cymbellales but not to the Gomphonemataceae. In addition, molecular data put Gomphoneis tegelensis R.Jahn & N.Abarca also into Gomphonella. In order to make the genera Gomphoneis and Gomphonema monophyletic, their astigmate members are transferred to Gomphonella.

Conclusions – The results clarify that the gomphonemoid outline is not restricted to the family Gomphonemataceae but seem to be distributed across the entire order Cymbellales. This is shown in this paper for the revived genus Gomphonella, which contains the astigmate group of Gomphoneis and Gomphonema besides the longly disputed G. olivacea. Only a polyphasic approach, combining molecular and micromorphological data for taxonomy, nomenclatural evaluation, and observations from clonal cultures can reveal the full intricacies of evolutionary relations.

Keywords
Bacillariophyceae, diatoms, genus emendation, Gomphoneis, Gomphonema, nomenclatural types, phylogeny, polyphasic approach

References

  • Agardh C.A. (1824) Systema algarum. Literis Berlingianis.
  • Agardh C.A. (1830) Conspectus criticus diatomacearum. Lund. 1–2: 1–38.
  • Boyer C.S. (1928) Synopsis of North American Diatomaceae 2. Proceedings of the Academy of Natural Sciences of Philadelphia 79, suppl.: 1–583.
  • Brébisson A. de, Godey L.L. (1835) Algues des environs de Falaise. Falaise, De Brée l’ainé.
  • Brébisson A. de (1838) Considérations sur les diatomées. Falaise, De Brée l’ainé, Paris, Meilhac.
  • Brinkmann N., Hodač L., Mohr K.I., Hodačová A., Jahn R., Ramm J., Hallmann C., Arp G., Friedl T. (2015) Cyanobacteria and diatoms in biofilms of two karstic streams in Germany and changes of their communities along calcite saturation gradients. Geomicrobiology Journal 32: 255–274. https://doi.org/10.1080/01490451.2014.901438
  • Brun J.-J. (1880) Diatomées des Alpes et du Jura et de la région Suisse et Française des environs de Genève. Genève, H. Georg, Paris Georges Masson.
  • Cleve P.T. (1868) Svenska och Norska Diatomacéer. Öfversigt af Kongl. Vetenskaps-Akademiens förhandlingar. Stockholm 25(3): 213–240, pl. 4.
  • Cleve P.T. (1894) Synopsis of the naviculoid diatoms. Kongliga Svenska Vetenskaps Academiens Handlingar 26: 1–96.
  • Cox E.J. (2015) Diatoms, Diatomeae (Bacillariophyceae s.l., Bacillariophyta). In: Frey W. (ed.) Syllabus of plant families 2/1. Photoautotrophic eukaryotic Algae: 64–103. Stuttgart, Borntraeger Science Publishers.
  • Crossetti L.O., Stenger-Kovács C., Padisák J. (2013) Coherence of phytoplankton and attached diatom-based ecological status assessment in Lake Balaton. Hydrobiologia 716(1): 87–101. https://doi.org/10.1007/s10750-013-1547-0
  • Le Cohu R., Coste M. (1995) Le genre Gomphoneis (Bacillariophyta): un nouveau modèle d’organisation du cingulum. Canadian Journal of Botany 73: 112–120. https://doi.org/10.1139/b95-013
  • Droege G., Barker K., Astrin J., Bartels P., Butler C., Cantrill D., Coddington J., Forest F., Gemeinholzer B., Hobern D., Mackenzie-Dodds J., Ó Tuama É., Petersen G., Sanjur O., Schindel D., Seberg O. (2014) The Global Genome Biodiversity Network (GGBN) Data Portal. Nucleic Acids Research. 42(D1): D607-D612. https://doi.org/10.1093/nar/gkt928
  • Ehrenberg C.G. (1830) Beiträge zur Kenntniss der Organisation der Infusorien und ihrer geographischen Verbreitung, besonders in Sibirien. Abhandlungen der Königlichen Akademie der Wissenschaften in Berlin 1830: 1–87, Tafeln I–VIII.
  • Ehrenberg C.G. (1832) Über die Entwicklung und Lebensdauer der Infusionsthiere nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Systeme. Abhandlungen der Königlichen Akademie der Wissenschaften in Berlin 1831: 1–154, Tafeln 1–4.
  • Güntsch A., Hyam R., Hagedorn G., Chagnoux S., Röpert D., Casino A., Droege G., Glöckler F., Gödderz K., Groom Q., Hoffmann J., Holleman A., Kempa M., Koivula H., Marhold K., Nicolson N., Smith V.S, Triebel D. (2017) Actionable, long-term stable and semantic web compatible identifiers for access to biological collection objects. Database (Oxford) 2017(1): bax003. https://doi.org/10.1093/database/bax00
  • Hofmann G., Werum M., Lange-Bertalot H. (2013) Diatomeen im Süßwasser-Benthos von Mitteleuropa. Bestimmungsflora Kieslealgen für die ökologische Praxis. Über 700 der häufigsten Arten und ihre Ökologie. [1]–908. Königstein, Koeltz Scientific Books.
  • Hornemann J.W. (1810) Flora Danica 8(24): [1]–6, pls 1381–1440.
  • Hustedt F. (1945) Diatomeen aus Seen und Quellgebieten der Balkanhalbinsel. Archiv für Hydrobiologie 40: 867–973.
  • Index Nominum Genericorum (2018) University Herbarium, University of California, Berkeley. Compiled by Paul Silva [online]. Available from http://ucjeps.berkeley.edu/CPD/ [accessed 24 Sep 2018].
  • Jahn R., Abarca N., Gemeinholzer B., Mora D., Skibbe O., Kulikovskiy M., Gusev E., Kusber W.-H., Zimmermann J. (2017) 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. https://doi.org/10.1080/0269249X.2017.1312548
  • Jahn R., Kusber W.-H. (continuously updated) AlgaTerra Information System [online]. Botanic Garden and Botanical Museum Berlin, Freie Universität Berlin. Available from: http://www.algaterra.org [accessed 24 Sep. 2018].
  • Kermarrec L., Ector L., Bouchez A., Rimet F., Hoffmann L. (2011) A preliminary phylogenetic analysis of the Cymbellales based on 18S rDNA gene sequencing. Diatom Research 26: 305–315. https://doi.org/10.1080/0269249X.2011.633255
  • Kociolek J.P. (2011) Gomphoneis olivaceum. In Diatoms of the United States [online]. Available from http://westerndiatoms.colorado.edu/taxa/species/gomphoneis_olivaceum [accessed 24 Sep. 2018].
  • Kociolek J.P., Stoermer E.F. (1988a) Taxonomy, ultrastructure, and distribution of Gomphoneis herculeana, G. eriense and closely related species. Proceedings of the Academy of Natural Sciences of Philadelphia 140: 24–97.
  • Kociolek J.P., Stoermer E.F. (1988b) Observations on North American Gomphoneis (Bacillariophyceae). IV. Valve ultrastructure and systematic position of Gomphoneis elegans. Transactions of the American Microscopical Society 107: 386–396.
  • Kociolek J.P., Stoermer E.F. (1988c) A preliminary investigation of the phylogenetic relationships among the freshwater, apical pore field-bearing cymbelloid and gomphonemoid diatoms (Bacillariophyceae) 1. Journal of Phycology 24: 377–385. https://doi.org/10.1111/j.1529-8817.1988.tb04480.x
  • Kociolek J.P., Stoermer E.F. (1989) Phylogenetic relationships and evolutionary history of the diatom genus Gomphoneis. Phycologia 28: 438–454.
  • Kociolek J.P., You Q.-M., Wang Q.-X., Liu Q. (2015) A consideration of some interesting freshwater gomphonemoid diatoms from North America and China, and the description of Gomphosinica gen. nov. Nova Hedwigia, Beiheft 144: 175–198.
  • Krammer K., Lange-Bertalot H. (1985) Naviculaceae. Neue und wenig bekannte Taxa, neue Kombinationen und Synonyme sowie Bemerkungen zu einigen Gattungen. Bibliotheca Diatomologica 9: 1–230. Berlin & Stuttgart, J. Cramer.
  • Krammer K., Lange-Bertalot H. (1991) Bacillariophyceae. 4. Teil: Achnanthaceae. Kritische Ergänzungen zu Navicula (Lineolatae) und Gomphonema. In: Ettl H., Gärtner G., Gerloff J., Heynig H., Mollenhauer D. (eds) Süßwasserflora von Mitteleuropa 2/4. Stuttgart & Jena, Gustav Fischer,.
  • Kützing F.T. (1833) Synopsis Diatomacearum oder Versuch einer systematischen Zusammenstellung der Diatomeen. Linnaea 8: 529–620, Tafeln XIII–XIX.
  • Lange-Bertalot H. (1993) 85 Neue Taxa und über 100 weitere neu definierte Taxa ergänzend zur Süßwasserflora von Mitteleuropa Vl. 2/1–4. Bibliotheca Diatomologica 27: 1–454. Berlin & Stuttgart, J. Cramer.
  • Leiblein V. (1830) Algologische Bemerkungen. Flora 13: 305–318, 323–335, 337–351.
  • Levkov Z., Krstic S., Metzeltin D., Nakov T. (2007) Diatoms of Lakes Prespa and Ohrid, about 500 taxa from ancient lake system. Iconographia Diatomologica 16: 1–613.
  • Levkov Z., Mitić-Kopanja D., Reichardt E. (2016) The diatom genus Gomphonema from the Republic of Macedonia. In: Lange-Bertalot H. (ed.) Diatoms of Europe 8. Oberreifenberg, Koeltz Botanical Books.
  • Li Y.L., Shi Z.X., Xie P. (2003) New varieties of Gomphonema and Cymbella (Bacillariophyta) from Qinghai Province. Acta Hydrobiologica Sinica 27: 147–148.
  • Lyngbye H.C. (1819) Tentamen hydrophytologiae danicae continens omnia hydrophyte cryptogama Daniae, Holsatiae, Faeroae, Islandiae, Groenlandiae hucusque cognita, systematice disposita, descripta et iconibus illustrata, adjectis simul speciebus norvegicis. Copenhagen, Schultz. https://doi.org/10.5962/bhl.title.6079
  • Miller M.A., Pfeiffer W., Schwartz T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE).New Orleans & Los Angeles, GCE. https://doi.org/10.1109/GCE.2010.5676129
  • Mora D., Carmona J., Jahn R., Zimmermann J., Abarca N. (2017) Epilithic diatom communities of selected streams from the Lerma–Chapala Basin, Central Mexico, with the description of two new species. PhytoKeys 88: 39–69. https://doi.org/10.3897/phytokeys.88.14612
  • Müller J., Müller K., Neinhuis C., Quandt D. (2010) PhyDE®–Phylogenetic data editor. Computer program. Available from: http://www.phyde.de/ [accessed 11 Mar. 2019].
  • Nakov T., Ruck E.C., Galachyants Y., Spaulding S.A., Theriot E.C. (2014) Molecular phylogeny of the Cymbellales (Bacillariophyceae, Heterokontophyta) with a comparison of models for accommodating rate variation across sites. Phycologia 53: 359–373.
  • Pantocsek J. (1889) Beiträge zur Kenntnis der Fossilen Bacillarien Ungarns. Teil II. Brackwasser Bacillarien. Anhang: Analyse de marine Depots von Bory, Bremia, Nagy-Kurtos in Ungarn; Ananio und Kusnetzk in Russland. Nagy-Tapolcsány, Nagy-Kürtös, Julius Platzko.
  • Pantocsek J. (1893 „1892“) Beiträge zur Kenntniss der Fossilen Bacillarien Ungarns III. Süsswasser Bacillarien. Nagy-Tapolcsány, Julius Platzko.
  • Pantocsek J. (1901) A Balaton Kovamoszatai vagy Bacillariái. Budapest.
  • Phycobank (continuously updated) Phycobank: registration of nomenclatural acts of algae [online]. Available from https://www.phycobank.org [accessed 24 Sep. 2018].
  • Rambaut A. (2008) Figtree version 1.2.2. Insitute of Evolutionary Biology, University of Edinburgh. Available from: http://tree.bio.ed.ac.uk/software/figtree [accessed 11 Mar. 2019].
  • Reichardt E. (2015) The identity of Gomphonema clavatum Ehrenberg (Bacillariophyceae) and typification of five species of the genus Gomphonema described by C.G. Ehrenberg. Diatom Research 30: 141–149. https://doi.org/10.1080/0269249X.2015.1009386
  • Ross R., Sims P.A. (1978) Notes on some diatoms from the Isle of Mull, and other Scottish localities. Bacillaria 1: 151–168.
  • Round F.E., Crawford R.M., Mann D.M. (1990) The diatoms. Biology & morphology of the genera. Cambridge, Cambridge University Press.
  • Schneider O. (1878) Naturwissenschaftliche Beiträge zur Kenntniss der Kaukasusländer: auf Grund seiner Sammelbeute. Dresden, Burdach.
  • Skibbe O., Zimmermann J., Kusber W.-H., Abarca N., Buczkó K., Jahn R. (2018) Gomphoneis tegelensis sp. nov. (Bacillariophyceae): a morphological and molecular investigation based on selected single cells. Diatom Research 33: 251–262. https://doi.org/10.1080/0269249X.2018.1518835
  • Spaulding S., Edlund M. (2009) Gomphoneis. In: Diatoms of North America [online]. Available from https://diatoms.org/genera/gomphoneis [accessed 24 Sep. 2018].
  • 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. https://doi.org/10.1093/molbev/mst197
  • Tavaré S. (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17: 57–86.
  • Turland N.J., Wiersema J.H., Barrie F.R., Greuter W., Hawksworth D.L., Herendeen P.S., Knapp S., Kusber W.-H., Li D.-Z., Marhold K., May T.W., McNeill J., Monro A.M., Prado J., Price M.J., Smith G.F. (eds) (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Glashütten, Koeltz Botanical Books. https://doi.org/10.12705/Code.2018
  • Van Heurck H. (1880) Synopsis des diatomées de Belgique. Atlas. Anvers.
  • Werum M., Lange-Bertalot H. (2004) Diatoms in springs from Central Europe and elsewhere under the influence of hydrogeology and anthropogenic impacts. Iconographia Diatomologica 13: 3–417. Ruggell, Gantner.
  • Vázquez G., Aké-Castillo J.A., Favila M.E. (2011) Algal assemblages and their relationship with water quality in tropical Mexican streams with different land uses. Hydrobiologia 667: 173–189. https://doi.org/10.1007/s10750-011-0633-4
  • 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. https://doi.org/10.1007/s13127-011-0050-6
  • 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. https://doi.org/10.1371/journal.pone.0108793