Morphological and molecular characterization of twenty-five new Diploneis species (Bacillariophyta) from Lake Tanganyika and its surrounding areas

ELENA JOVANOVSKA; MALLORY C. WILSON; PAUL B. HAMILTON; JEFFERY STONE

doi:10.11646/phytotaxa.593.1.1

Issue: Vol. 593 No. 1: 21 April 2023

Type: Monograph

Published: 2023-04-21

DOI: 10.11646/phytotaxa.593.1.1

Page range: 1-102

Abstract views: 169

PDF downloaded: 5

**Morphological and molecular characterization of twenty-five new Diploneis species (Bacillariophyta) from Lake Tanganyika and its surrounding areas**

ELENA JOVANOVSKA⁺⁻
MALLORY C. WILSON⁺⁻
PAUL B. HAMILTON⁺⁻
JEFFERY STONE⁺⁻

Department of Paleoanthropology, Senckenberg Research Institute and Natural History Museum Frankfurt, Frankfurt, Germany

Indiana State University, Indiana State University, Terre Haute, IN, USA

Phycology Section, Research and Collections Division, Canadian Museum of Nature, Ottawa, Canada

Indiana State University, Indiana State University, Terre Haute, IN, USA

ancient lake morphology multi-locus phylogeny species richness taxonomy Algae

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Abstract

Lake Tanganyika, the second oldest lake in the world, is home to some of the largest and most phenotypically, genetically, and ecologically diverse freshwater assemblages. While the evolutionary processes responsible for generating its extraordinary richness are well understood across various animal groups, little is known about the diatom species richness, turnover patterns, and their drivers. Here, we explored species richness of the diatom genus Diploneis from Lake Tanganyika and surrounding regions by using morphological and molecular information. Both datasets suggested the presence of twenty-five new Diploneis species, each not related to any known Diploneis species so far. The multi-locus phylogeny indicates a monophyletic group of twenty-one Diploneis species from Lake Tanganyika, suggesting potential intralacustrine diversification possibly triggered by certain historical contingencies. This is supported by the small genetic distances and the presence of unique silica ornamentations on the valve face exterior, to date only known to occur on the Baikal endemic Diploneis implicatus. The discovery of such a high richness of Diploneis species in Lake Tanganyika and the presence of a unique morphological character points to a potential adaptive radiation - a mechanism yet to be confirmed.

References

Ashworth, M.P., Lobban, C.S., Witkowski, A., Theriot, E.C., Sabir, M.J., Baeshen, M.N., Hajarah, N.H., Baeshen, N.A., Sabir, J.S. & Jansen, R.K. (2016) Molecular and morphological investigations of the stauros-bearing, raphid pennate diatoms (Bacillariophyceae): Craspedostauros E. J. Cox, and Staurotropis T.B.B. Paddock, and their relationship to the rest of the Mastogloiales. Protist 168: 48–70. https://doi.org/10.1016/j.protis.2016.11.001
Bory de Saint-Vincent, J.B.G.M. (1822) Bacillarées. Dictionnaire Classique D’histoire Naturelle 2: 127–129.
Bramburger, A.J., Haffner, G.D. & Hamilton, P.B. (2004) Examining the distributional patterns of the diatom flora of the Malili Lakes, Sulawesi, Indonesia. In: Poulin, M. (Ed.) Proceedings of the 17th International Diatom Symposium. Biopress Limited, Bristol, U.K., pp. 11–25.
Cleve, P.T. (1891) The diatoms of Finland. Acta Societatia pro Fauna et Flora Fennica 8 (2): 1–68.
Cleve, P.T. (1894) Synopsis of the naviculoid diatoms. Part I. Kongliga Svenska Vetenskapsakademiens Handlingar Series 4 26 (2): 1–194.
Cocquyt, C. (1998) Diatoms from the northern basin from Lake Tanaganyika. Bibliotheca Diatomologica 39: 7–275. https://doi.org/10.1127/nova.hedwigia/68/1999/425
Cocquyt, C. (1999) Diatoms from a hot spring in Lake Tanganyika. Nova Hedwigia 68: 425–439. https://doi.org/10.1127/nova.hedwigia/68/1999/425
Cocquyt, C. & Vyverman, M. (1994) Composition and diversity of the algal flora in the East African Great Lakes: a comparative survey of lakes Tanganyika, Malawi (Nyasa) and Victoria. Archiv für Hydrobiologie–Beiheft Ergebnisse der Limnologie 44: 161–172.
Cocquyt, C., Vyverman, W. & Compère, P. (1993) A check-list of the algal flora of the East African Great Lakes (Malawi, Tanganyika and Victoria). Scripta Botanica Belgica 8: 1–55.
Cohen, A.S., Bills, R., Cocquyt, C.Z. & Caljon, A.G. (1993) The impact of sediment pollution on biodiversity on Lake Tanganyika. Conservation Biology 7 (3): 667–677. 
Cohen, A.S. & Salzburger, W. (2017) Scientific Drilling at Lake Tanganyika, Africa: A Transformative Record for Understanding Evolution in Isolation and the Biological History of the African Continent, University of Basel, 6–8 June 2016. Scientific Drilling 22: 43–48. https://doi.org/10.5194/sd-22-43-2017
Coulter, G.W. (1991) Lake Tanganyika and its Life. Oxford U. Press.
Delandmeter, P., Lambrechts, J., Legat, V., Vallaeys, V., Naithani, J., Thiery, W., Remacle, J.-F. & Deleersnijder, E. (2018) A fully consistent and conservative 3D discontinuous Galerkin finite element model using a vertically adaptive mesh, with an application to the oscillations of the thermocline of a deep, elongated lake. Geoscientific Model Development 11: 1161–1179. https://doi.org/10.5194/gmd-11-1161-2018
De Wever, A., Muylaert, K., Van Der Gucht, K., Pirlot, S., Cocquyt, C., Descy, J.-P., Plisnier, P.-D. & Vyverman, W. (2005) Bacterial community composition in Lake Tanganyika: Vertical and horizontal heterogeneity. Applied and Environmental Microbiology 71: 5029–5037. https://doi.org/10.1128/AEM.71.9.5029-5037.2005
Docquier, D., Thiery, W., Lhermitte, S. & Lipzig, N. (2016) Multi-year wind dynamics around Lake Tanganyika. Climate Dynamics 47: 3191–3202. https://doi.org/10.1007/s00382-016-3020-z
Droop, S.J.M. (1998) Diploneis sejuncta (Bacillariophyta) and some new species from an ancient lineage. Phycologia 37 (5): 340–356. https://doi.org/10.2216/i0031-8884-37-5-340.1
Ehrenberg, C.G. (1832) Über die Entwicklung und Lebensdauer der Infusionsthiere; nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Systeme. Abhandlungen der Königlichen Akademie Wissenschaften zu Berlin, Physikalische Klasse 154 pp.
Evans, K.M., Wortley, A.H., Simpson, G.E., Chepurnov, V.A. & Mann, D.G. (2008) Molecular systematic approach to explore diversity within the Sellaphora pupula species complex (Bacillariophyta). Journal of Phycology 44 (1): 215–231. https://doi.org/10.1111/j.1529-8817.2007.00454.x.
Hamilton, P.B., Lefebvre, K.E. & Bull, R.D. (2015) Single cell PCR amplification of diatoms using fresh and preserved samples. Frontiers in Microbiology 6: 1084. https://doi.org/10.3389/fmicb.2015.01084
Hustedt, F. (1930) Bacillariophyta (Diatomeae) Zweite Auflage. In: Die Süsswasser-Flora Mitteleuropas. Heft 10. (Pascher, A. Eds), pp. [i]-vii, [1]–466. Jena: Verlag von Gustav Fischer.
Hustedt, F. (1935) Untersuchungen über den Bau der Diatomeen. X. Die sogenannten “Längslinien” in der Schalenstruktur pennater Diatomeen. XI. Strukturtypen in der Gattung Diploneis. Bericht der Deutschen Botanischen Gesellschaft 53 (1): 3–41.
Hustedt, F. (1937) Die Kieselalgen Deutschlands, Österreichs und der Schweiz unter Berücksichtigung der übrigen Länder Europas sowie der angrenzenden Meeresgebiete. Bd. VII: Teil 2: Lieferung 5. In: Anon. (Eds.) Rabenhorst’s Kryptogamen Flora von Deutschland, Österreich und der Schweiz., Leipzig: Akademische Verlagsgesellschaft. pp. 577–736.
Idei, M. (2013) Three new species of freshwater Diploneis from Japan. Diatom Research 28 (1): 1–11. https://doi.org/10.1080/0269249X.2012.734527
Jovanovska, E., Nakov, T. & Levkov, Z. (2013) Observations of the genus Diploneis (Ehrenberg) Cleve from Lake Ohrid, Macedonia. Diatom Research 28: 237–262. https://doi.org/10.1080/0269249X.2013.797219
Jovanovska, E., Levkov, Z. & Edlund, M.B. (2015) The genus Diploneis Ehrenberg ex Cleve (Bacillariophyta) from Lake Hövsgöl, Mongolia. Phytotaxa 217 (3): 201–248. https://doi.org/10.11646/phytotaxa.217.3.1
Jurilj, A. (1954) Flora i vegetacija Dijatomeja Ohridskog Jezera. Flora and vegetation of Diatoms from Ochrida Lake in Yugoslavia. J. Prirodnoslovnih Istraživanja 26: 99–190.
Kozlov, A.M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35: 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Kulikovskiy, M.S., Lange-Bertalot, H. & Kuznetsova, I.V. (2015) Lake Baikal: hotspot of endemic diatoms II. Iconographia Diatomologica 26: [1]–656. 
Kützing, F.T. (1844) Die Kieselschaligen Bacillarien oder Diatomeen. Nordhausen: zu finden bei W. Köhne [i–vii], pp. 1–152.
Lange-Bertalot, H., Metzeltin, D. & Witkowski, A (1996) Hippodonta gen. nov. Umschreibung und Begründung einer neuer Gattung der Naviculaceae. Iconographia Diatomologica 4: 247–275.
Lange-Bertalot, H., Fuhrmann, A. & Werum, M. (2020) Freshwater Diploneis: species diversity in the Holarctic and spot checks from elsewhere. In: Lange-Bertalot, H. (Ed.) Diatoms of Europe. Diatoms of European inland water and comparable habitats. Freshwater Diploneis Two studies, Glashütten: Koeltz Botanical Books. pp. 1–526, 691–699. 
Lange-Bertalot, H. & Fuhrmann, A. (2016) Contribution to the genus Diploneis (Bacillariophyta): twelve species from Holarctic freshwater habitats proposed as new to science. Fottea Olomouc 16 (2): 157–183. https://doi.org/10.5507/fot.2015.027
Lange-Bertlot, H. & Fuhrmann, A. (2017) Diploneis lecohuiana sp. nov., D. fereparma sp. nov. and D. parma Cleve: rare diatoms (Bacillariophyta) in Central European freshwater. Nova Hedwigia Beiheft 146: 33–42. 
 DOI 10.1127/1438-9134/2017/033
Levkov, Z. (2009) Amphora sensu lato. In: Lange-Bertalot, H. (Ed.) Diatoms of Europe: Diatoms of the European Inland Waters and Comparable Habitats. Vol. 5, Ruggell: A.R.G. Gantner Verlag K.G. pp. 916. 
Levkov, Z. & Williams, D. (2012) Checklist of diatoms (Bacillariophyta) from Lake Ohrid and Lake Prespa (Macedonia), and their watersheds. Phytotaxa 45: 1–76. https://doi.org/10.11646/phytotaxa.45.1.1
Liu, Y., Kociolek, J.P., Fan, Y. & Wang, Q. (2012) Pseudofallacia gen. nov., a new freshwater diatom (Bacillariophyceae) genus based on Navicula occulta Krasske. Phycologia 51 (6): 620–626. https://doi.org/10.2216/11-098.1
Lobban, C.S., Majewska, R., Ashworth, M., Bizsel, N., Bosak, S., Kooistra, W.H.C.F., Lam, D.W., Navarro, J.N., Pennesi, C., Sato, S., Van de Vijver, B. & Witkowski, A. (2021) Diatom genus Hyalosira (Rhabdonematales emend.) and resolution of its polyphyly in Grammatophoraceae and Rhabdonemataceae with a new genus, Placosira, and five new Hyalosira species. Protist 172 (3): 125816. https://doi.org/10.1016/j.protis.2021.125816
Meister, F. (1912) Die Kieselalgen der Schweiz. Beitrage zur Kryptogamenflora der Schweiz. Matériaux pour la flore cryptogamique suisse. pp. 254.
Mereschkowsky, C. (1902) On Sellaphora, a new genus of diatoms. Annals and Magazine of Natural History Series 7 9: 185–195.
Metzeltin, D., Lange-Bertalot, H. & Soninkhishig, N. (2009) Diatoms in Mongolia. Iconographia Diatomologica 20: [1] –686.
Nakov, T., Beaulieu, J.M. & Alverson, A.A. (2018) Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta). New Phytologist 219: 462–473. https://doi.org/10.1111/nph.15137
Patrick, R. & Reimer, C.W. (1966) The diatoms of the United States exclusive of Alaska and Hawaii. Volume 1: Fragilariaceae, Eunotiaceae, Achnanthaceae, Naviculaceae. Monographs of the Academy of Natural Sciences of Philadelphia 13. pp. 688.
Nawrocki, E.P. (2009) Structural RNA homology search and alignment using covariance models (Ph.D. thesis). Washington University in Saint Louis, School of Medicine. https://doi.org/10.7936/K78050MP
Pappas, J.L., Kociolek, J.P. & Stoermer, E.F. (2014) Quantitative morphometric methods in diatom research. Nova Hedwigia Beihefte 143: 281–306. https://doi.org/10.1127/1436-7270/2014/015
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256. https://doi.org/10.1093/molbev/msn083
Rabenhorst, L. (1864) Flora europaea algarum aquae dulcis et submarinae. Sectio I. Algas diatomaceas complectens, cum figuris generum omnium xylographice impressis. Lipsiae [Leipzig]: Apud Eduardum Kummerum, pp. 359.
Rodionova, Y., Pomazkina, G. & Sherbakova, T. (2019) Three new diatom species of the genus Diploneis (Bacillariophyta) from Lake Baikal. Diatom Research 34 (2): 95–108. https://doi.org/10.1080/0269249X.2019.1620339
Rambaut, A. & Drummond, A.J. (2007) Tracer v. 1.5. Available from: http://tree.bio.ed.ac.uk/software/tracer (accessed 20 April 2023)
Reichardt, E. (2004) Eine bemerkenswerte Diatomeenassoziation in einem Quellhabitat im Grazer Bergland, Österreich. Ein Beitrag zur Kenntnis seltener und wenig bekannter Diatomeen. Iconographia Diatomologica 13: 418–479.
Renberg, I. (1990) A procedure for preparing large sets of diatom slides from sediment cores. Journal of Paleolimnology 4: 87–90. https://doi.org/10.1007/BF00208301
Ring, U., Albrecht, C. & Schrenk, F. (2018) The East African Rift System: Tectonics, Climate and Biodiversity. In: Mountains, Climate and Biodiversity. Publisher: Wiley Blackwell, pp. 391–411.
Ronco, F., Matschiner, M., Böhne, A., Boila, A., Büscher, H.H., El Taher, A., Indermaur, A., Malinsky, M., Ricci, V., Kahmen, A., Jentoft, S. & Salzburger, W. (2021) Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature 589: 76–81. https://doi.org/10.1038/s41586-020-2930-4
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, A.M. & Huelsenbeck, P.J. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.
Round, F.E., Crawford, R.M. & Mann, D.G. (1990) The diatoms. Biology and morphology of the genera. Cambridge University Press, Cambridge, pp. 747.
Russell, J. M., Barker, P., Cohen, A., Ivory, S., Kimirei, I., Lane, C., Leng, M., Maganza, N., McGlue, M., Msaky, E., Noren, A., Park Boush, L., Salzburger, W., Scholz, C., Tiedemann, R., Nuru, S. & the Lake Tanganyika Scientific Drilling Project (TSDP) Consortium (2020) ICDP workshop on the Lake Tanganyika Scientific Drilling Project: a late Miocene–present record of climate, rifting, and ecosystem evolution from the world’s oldest tropical lake. Scientific drilling: reports on deep earth sampling and monitoring, 27: 53–60. https://doi.org/10.5194/sd-27-53-2020
Sabir, J.S., Theriot, E.C., Manning, S.R., Al-Malki, A.L., Khiyami, M.A., Al-Ghamdi, A.K., Sabir, M.J., Romanovicz, D.K., Hajrah, N.H., El Omri, A., Jansen, R.K. & Ashworth, M.P. (2018) Phylogenetic analysis and a review of the history of the accidental phytoplankter, Phaeodactylum tricornutum Bohlin (Bacillariophyta). PLoS ONE 13: e0196744. https://doi.org/10.1371/journal.pone.0196744
Salzburger, W. (2018) Understanding explosive diversification through cichlid fish genomics. Nature Reviews Genetics 19 (11): 705–717. https://doi.org/10.1038/s41576-018-0043-9
Salzburger, W., van Bocxlaer, B. & Cohen, A.S. (2014) The ecology and evolution of the African Great Lakes and their faunas. Annual Review of Ecology, Evolution, and Systematics 45 (1): 519–545. https://doi.org/10.1146/annurev-ecolsys-120213-091804
Schluter, D. (2000) The ecology of adaptive radiation. OUP Oxford.
Skvortzow, B. & Meyer, C. (1928) A contribution to the Diatoms of Baikal Lake. Proceedings of the Sungaree River Biological Station 1 (5): 1–55.
Stelbrink, B., Jovanovska, E., Levkov, Z., Ognjanova-Rumenova, N., Wilke, T. & Albrecht, C. (2018) Diatoms do radiate: evidence for a freshwater species flock. Journal of Evolutionary Biology 31: 1969–1975. https://doi.org/10.1111/jeb.13368
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. The Society for Molecular Biology and Evolution, Oxford University, Oxford.
Theriot, E.C., Ashworth, M., Ruck, E., Nakov, T. & Jansen, R.K. (2010) A preliminary multigene phylogeny of the diatoms (Bacillariophyta): challenges for future research. Plant Ecology and Evolution 143: 278–296. https://doi.org/10.5091/plecevo.2010.418
Turpin, P.J.F. (1828) Observations sur le nouveau genre Surirella. Mémoires du Musée d’Histoire Naturelle 16: 361–368.
Van Meel, L. (1954) Le phytoplancton. In: Résultats scientifiques de l’exploration hydrobiologique du lac Tanganika (1946–1947) 4 (1), Bruxelles, Institut Royal des Sciences Naturelles de Belgique, A. pp. 681, B. 76 pl.
Werum, M. & Lange-Bertalot, H. (2004) Diatoms in springs, from Central Europe and elsewhere under the influence of hydrogeology and anthropogenic impages. Iconographia Diatomologica 13. pp. 1–417.
West, G.S. (1907) Report on the freshwater algae, including phytoplankton of the Third Tanganyika Expedition, conducted by Dr. W.A. Cunnington 1904–1905. Journal of the Linnean Society of London Botany 38: 81–197.
Wilke, T., Wagner, B., van Bocxlaer, B., Albrecht, C., Ariztegui, D., Delicado, D., Francke, A., Harzhauser, M., Hauffe, T., Holtvoeth, J., Just, J., Leng, J.M., Levkov, Z., Penkman, K., Sadori, L., Skinnern, A., Stelbrink, B., Vogel, H. & Wonik, T. (2016) Scientific drilling projects in ancient lakes: Integrating geological and biological histories. Global and Planetary Change 143: 118–151. https://doi.org/10.1016/j.gloplacha.2016.05.005
Wilke, T., Hauffe, T., Jovanovska, E., Cvetkoska, A., Donders, T., Ekschmitt, K., Francke, A., Lacey, J.H., Levkov, Z., Marshall, C.R., Neubauer, T.A., Silvestro, D., Stelbrink, B., Vogel, H., Albrecht, C., Holtvoeth, J., Krastel, S., Leicher, N., Leng, M.J., Lindhorst, K., Masi, A., Ognjanova-Rumenova, N., Panagiotopoulos, K., Reed, J.M., Sadori, L., Tofilovska, S., van Bocxlaer, B., Wagner-Cremer, F., Wesselingh, F.P., Wolters, V., Zanchetta, G., Zhang, X. & Wagner, B. (2020) Deep drilling reveals unexpected decreasing extinction rate after formation of ancient ecosystem. Science Advances 6: eabb2943. https://doi. org/10.1126/sciadv.abb2943
Woodard, K. & Neustupa, J. (2016) Morphometric asymmetry of frustule outlines in the pennate diatom Luticola poulickovae (Bacillariophyceae). Symmetry (Basel) 8: 6–9. https://doi.org/10.3390/sym8120150