Molecular phylogenetic analyses place Ardissonea crystallina (C. Agardh) Grunow and all Toxariids among the bi- and multipolar centric diatoms, almost always recovered as a derived lineage sister to Lampriscus. In all centrics where sexual reproduction has been documented, oogamy, with larger immobile eggs and smaller flagellated sperm has been observed. We were able to initiate both homothallic and heterothallic reproduction in A. crystallina. The heterothallic reproduction turned out to be non-oogamous; gametes were more or less equal in size but no flagellated cells were detected. At the same time, two mating types ("male" and "female") were recognized by the distinct morphology and behaviour of the gametes. While no flagella were observed, periodically thin cytoplasmic projections arose on the surface of the "male" gametes. These projections similar to those found in some pennate diatoms facilitated contact with the "female" cells. In each gametangial cell, regardless of the mating type, only one gamete was formed. Thus, the Toxariids may represent a unique evolutionary group, at least in respect to their reproductive biology. The hypothesis discussed is that non-oogamous mode of reproduction could have evolved in Ardissonea (and possibly in other Toxariids) independently of the pennate lineage of diatoms.

Department of Biology Mount Allison University Sackville New Brunswick E4L 1G7 Canada

Department of Botany Faculty of Science Palacký University in Olomouc Šlechtitelů 27 CZ 78371 Olomouc Czech Republic

MMS EA 2160 Faculté des Sciences et des Techniques Université du Maine Avenue Olivier Messiaen 72085 Le Mans Cedex 9 France

Natural Sciences Research and Educational Center and Palaeoceanology Unit Faculty of Geosciences University of Szczecin Mickiewicza 16a Szczecin 70 383 Poland

T 1 Vyasemsky Karadag scientific station Nature Reserve village Kurortnoe Feodosiya 298188 Russia

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Kirchner, O. Algen. In Kryptogamen-Flora von Schlesien. Zweiter Band. Erste Hälfte. 283 p. (Breslau,1878).

Round, F. E., Crawford, R. M. & Mann, D. G. The Diatoms. Biology and Morphology of the Genera. (Cambridge University Press, 1990).

Hustedt, B. Die Kieselalgen Deutschlands, Osterreichs und der Schweiz. In Kryptogamen-Flora von Deutschland, Osterreichs und der Schweiz. Vol. 2. (ed. Rabenhorst, L.) (Leipzig, 1961–1906).

Simonsen R. The diatom system: Ideas on phylogeny. Bacillaria. 1979;2:9–71.

Medlin LK, Kaczmarska I. Evolution of the diatoms: V. Morphological and cytological support for the major clades and a taxonomic revision. Phycologia. 2004;43:245–270. doi: 10.2216/i0031-8884-43-3-245.1. DOI

Kooistra WHCF, De Stefano M, Mann DG, Medlin LK. The phylogeny of the diatoms. Progr. Mol. Subcell. Biol. 2003;33:59–97. doi: 10.1007/978-3-642-55486-5_3. PubMed DOI

Adl SM, et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 2005;52:399–451. doi: 10.1111/j.1550-7408.2005.00053.x. PubMed DOI

Medlin LK, et al. Evolution of the diatoms. VI. Assessment of the new genera in the araphids using molecular data. Nova Hedwigia. 2008;133:81–100.

Theriot EC, Ashworth M, Ruck E, Nakov T, Jansen RK. A preliminary multigene phylogeny of the diatoms (Bacillariophyta): challenges for future research. Plant Ecol. Evol. 2010;143:278–296. doi: 10.5091/plecevo.2010.418. DOI

Pickett–Heaps JD, Hill DRA, Blaze KL. Active gliding motility in an araphid marine diatom, Ardissonea (formerly Synedra) crystallina. J. Phycol. 1991;27:718–725. doi: 10.1111/j.0022-3646.1991.00718.x. DOI

Kooistra WHCF, De Stefano M, Mann DG, Salma N, Medlin LK. Phylogenetic position of Toxarium, a pennate–like lineage within centric diatoms (Bacillariophyceae) J. Phycol. 2003;39:185–197. doi: 10.1046/j.1529-8817.2003.02083.x. DOI

Medlin LK, Sato S, Mann DG, Kooistra WHCF. Molecular evidence confirms sister relationship of Ardissonea, Climacosphenia, and Toxarium within the bipolar centric diatoms (Bacillariophyta, Mediophyceae), and cladistic analyses confirm that extremely elongated shape has arisen twice in the diatoms. J. Phycol. 2008;44:1340–1348. doi: 10.1111/j.1529-8817.2008.00560.x. PubMed DOI

Ashworth MP, Ruck EC, Lobban CS, Romanovicz DK, Theriot EC. A revision of the genus Cyclophora and description of Astrosyne gen. nov. (Bacillariophyta), two genera with the pyrenoids contained within pseudosepta. Phycologia. 2012;51:684–699. doi: 10.2216/12-004.1. DOI

Ashworth MP, Nakov T, Theriot EC. Revisiting Ross and Sims (1971): toward a molecular phylogeny of the Biddulphiaceae and Eupodiscaceae (Bacillariophyceae) J. Phycol. 2013;49:1207–1222. doi: 10.1111/jpy.12131. PubMed DOI

Theriot EC, Ashworth MP, Nakov T, Ruck E, Jansen RK. Dissecting signal and noise in diatom chloroplast protein encoding genes with phylogenetic information profiling. Mol. Phylogenet. Evol. 2015;89:28–36. doi: 10.1016/j.ympev.2015.03.012. PubMed DOI

Idei M, et al. Gametogenesis and auxospore development in Actinocyclus (Bacillariophyta) PLoS ONE. 2012;7(1–15):e41890. doi: 10.1371/journal.pone.0041890. PubMed DOI PMC

Geitler L. Der Formwechsel der pennaten Diatomeen (Kieselalgen) Arch. Protistenkd. 1932;78:1–226.

Geitler L. Reproduction and life history in diatoms. Bot. Rev. 1935;1:149–161. doi: 10.1007/BF02870149. DOI

Davidovich NA, Mouget J-L, Gaudin P. Heterothallism in the pennate diatom Haslea ostrearia (Bacillariophyta) Eur. J. Phycol. 2009;44:251–261. doi: 10.1080/09670260802710301. DOI

Davidovich NA, Gastineau R, Gaudin P, Davidovich OI, Mouget J-L. Sexual reproduction in the newly-described blue diatom, Haslea karadagensis. Fottea, Olomouc. 2012;12:219–229. doi: 10.5507/fot.2012.016. DOI

Kaczmarska I, Davidovich NA, Ehrman JM. Sex cells and reproduction in the diatom Nitzschia longissima (Bacillariophyta): discovery of siliceous scales in gamete cell walls and novel elements of the perizonium. Phycologia. 2007;46:726–737. doi: 10.2216/07-04.1. DOI

Sato S, Beakes G, Idei M, Nagumo T, Mann DG. Novel sex cells and evidence for sex pheromones in diatoms. PLoS ONE. 2011;6:e26923. doi: 10.1371/journal.pone.0026923. PubMed DOI PMC

Davidovich NA, et al. Mechanism of male gamete motility in araphid pennate diatoms from the genus Tabularia (Bacillariophyta) Protist. 2012;163:480–494. doi: 10.1016/j.protis.2011.09.002. PubMed DOI

Podunay YA, Davidovich OI, Davidovich NA. Mating system and two types of gametogenesis in the fresh water diatom Ulnaria ulna (Bacillariophyta) Algologia (in Russ) 2014;24:3–19. doi: 10.15407/alg24.01.003. DOI

Kaczmarska I, Gray BS, Jr, Ehrman JM, Thaler M. Sexual reproduction in plagiogrammacean diatoms: first insights into the early pennates. PLoS One. 2017;12:e0181413. doi: 10.1371/journal.pone.0181413. PubMed DOI PMC

Medlin LK. Opinion: Can coalescent models explain deep divergences in the diatoms and argue for the acceptance of paraphyletic taxa at all taxonomic hierarchies? Nova Hedwigia. 2016;102:107–128. doi: 10.1127/nova_hedwigia/2015/0295. DOI

Idei M, et al. Spermatogenesis and auxospore structure in the multipolar centric diatom. Hydrosera. J. Phycol. 2015;51:144–158. doi: 10.1111/jpy.12261. PubMed DOI

Idei, M. & Nagumo, T. Auxospore structure of the marine diatom genus Lampriscus with triangular/quadrangular forms. In Abstracts book of 17th International Diatom Symposium. (ed. Poulin, M.) p. 166 (Ottawa, Canada, 2002).

Sorhannus U. A nuclear–encoded small–subunit ribosomal RNA timescale for diatom evolution. Mar. Micropaleontol. 2007;65:1–12. doi: 10.1016/j.marmicro.2007.05.002. DOI

Stosch HAvon. Die Oogamie von Biddulphia mobiliensis und die bisher bekannten Auxosporenbildungen bei den Centrales. Rapp. Comm. VIIIème Congr. Int. Bot. Sect. 1954;17:58–68.

Stosch HA. von. Entwicklungsgeschichtliche Untersuchungen an zentrischen Diatomeen. II. Geschlechtszellenreifung, Befruchtung und Auxosporenbildung einiger grundbewohnender Biddulphiaceen der Nordsee. Arch. Mikrobiol. 1956;23:327–365. doi: 10.1007/BF00409861. PubMed DOI

Samanta, B., Kinney, M. E., Heffell, Q., Ehrman, J. M. & Kaczmarska, I. Gametogenesis and auxospore development in the bipolar centric diatom Brockmanniella brockmannii (family Cymatosiraceae). Protist., 10.1016/j.protis.2017.07.004 (2017). PubMed

Chepurnov VAW, et al. In search of new tractable diatoms for experimental biology. BioEssays. 2008;30:692–702. doi: 10.1002/bies.20773. PubMed DOI

Medlin, L. K. A review of the evolution of the diatoms from the origin of the lineage to their populations. In The Diatom World. Cellular Origin, Life in Extreme Habitats and Astrobiology. (eds Seckbach, J., Kociolek, J. P.) 19, 93–118 (Springer Science + Business Media B. V., 2011).

Sorhannus U, Fox MG. Phylogenetic analyses of a combined data set suggest that the Attheya lineage is the closest living relative of the pennate diatoms (Bacillariophyceae) Protist. 2011;163:252–262. doi: 10.1016/j.protis.2011.04.005. PubMed DOI

Kulikovskiy M, Lange–Bertalot H, Annenkova N, Gusev E, Kociolek JP. Morphological and molecular evidence support description of two new diatom species from the genus Ulnaria in Lake Baikal. Fottea, Olomouc. 2016;16:34–42. doi: 10.5507/fot.2015.011. DOI

Medlin LK. Evolution of the diatoms: VIII. Re–examination of the SSU–rRNA gene using multiple outgroups and a cladistic analysis of valve features. J Biodivers Biopros. Dev. 2014;1:129. doi: 10.4172/2376-0214.1000129. DOI

Medlin LK. Evolution of the diatoms: major steps in their evolution and a review of the supporting molecular and morphological evidence. Phycologia. 2016;55:79–103. doi: 10.2216/15-105.1. DOI

Sims PA, Mann DG, Medlin LK. Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia. 2006;45:361–402. doi: 10.2216/05-22.1. DOI

Diatomovyj analiz (ed A. I. Proshkina–Lavrenko) Vol. 1–3. (Moskva – Leningrad, 1949–1950).

Kociolek JP, Fourtanier E, Rubinstein J, Encinas A. Adoneis miocenica, a new species from Chile, with comments on the morphological separation of centric and pennate diatoms. Diatom Res. 2007;22:309–316. doi: 10.1080/0269249X.2007.9705717. DOI

Witkowski J, Sims PA, Harwood DM. Rutilariaceae redefined: a review of fossil bipolar diatom genera with centrally positioned linking structures, with implications for the origin of pennate diatoms. Eur. J. Phycol. 2011;46:378–398. doi: 10.1080/09670262.2011.629685. DOI

Theriot EC, Cannone JJ, Gutell RR, Alverson AJ. The limits of nuclear encoded SSU rDNA for resolving the diatom phylogeny. Eur. J. Phycol. 2009;44:277–290. doi: 10.1080/09670260902749159. PubMed DOI PMC

Rampen SW, et al. Phylogenetic position of Attheya longicornis and Attheya septentrionalis (Bacillariophyta) J. Phycol. 2009;45:444–453. doi: 10.1111/j.1529-8817.2009.00657.x. PubMed DOI

Schulz, P. Zur Auxosporenbildung von Thalassiosira baltica (Grun.) Ostenfeld Bericht Westpreussischen Botanisch–Zoologischen Vereins 52, 25–32 (1930).

Drebes G. Oogame Auxosporenbildung bei Thalassiosira eccentrica. Jahresbericht der Biol Anst. Helgoland. 1979;15:15–17.

Schmid, A. M. M. Wall morphogenesis in Thalassiosira eccentrica: comparison of auxospore formation and the effect of MT–inhibitors. In: Mann D. G., editor. Proceedings of the 7th International Diatom Symposium, Philadelphia, 1982 Koenigstein: O. Koeltz. p. 47–70 (1982).

Armbrust EV. Identification of a new gene family expressed during the onset of sexual reproduction in the centric diatom Thalassiosira weissflogii. Appl Environ Microbiol. 1999;65:3121–3128. PubMed PMC

Chepurnov VA, et al. Oogamous reproduction, with two–step auxosporulation, in the centric diatom Thalassiosira punctigera (Bacillariophyta) J. Phycol. 2006;42:845–858. doi: 10.1111/j.1529-8817.2006.00244.x. DOI

Dassow P, von Chepurnov VA, Armbrust EV. Relationships between growth rate, cell size, and induction of spermatogenesis in the centric diatom Thalassiosira weissflogii (Bacillariophyta) J. Phycol. 2006;42:887–899. doi: 10.1111/j.1529-8817.2006.00250.x. DOI

Mills KE, Kaczmarska I. Autogamic reproductive behavior and sex cell structure in Thalassiosira angulata (Bacillariophyta) Bot. Mar. 2006;49:417–430. doi: 10.1515/BOT.2006.053. DOI

Drebes G. Cell structure, cell division, and sexual reproduction of Attheya decora West (Bacillariophyceae, Biddulphiineae) Nova Hedwigia. 1977;54:167–178.

Stosch HA. von. On auxospore envelopes in diatoms. Bacillaria. 1982;5:127–156.

Kaczmarska I, Ehrman JM. Auxosporulation in Paralia guyana MacGillivary (Bacillariophyta) and possible new insights into the habit of the earliest diatoms. PLoS ONE. 2015;10:e0141150. doi: 10.1371/journal.pone.0141150. PubMed DOI PMC

Subba Rao DV, Partensky F, Wohlgeschaffen G, Li WKW. Flow cytometry and microscopy of gametogenesis in Nitzschia pungens, a toxic, bloom–forming, marine diatom. J. Phycol. 1991;27:21–26. doi: 10.1111/j.0022-3646.1991.00021.x. DOI

Subba Rao DV, Partensky F, Wohlgeschaffen G, Li WK. Comment. Gametogenesis in Nitzschia pungens f. multiseries. J. Phycol. 1992;28:574–576. doi: 10.1111/j.0022-3646.1992.00574.x. DOI

Fryxell GA, Garza SA, Roelke DL. Auxospore formation in an Antarctic clone of Nitzschia subcurvata Hasle. Diatom Res. 1991;6:235–245. doi: 10.1080/0269249X.1991.9705169. DOI

Rosowski, J. R., Johnson, L. M. & Mann D. G. On the report of gametogenesis, oogamy, and uniflagellated sperm in the pennate diatom Nitzschia pungens (1991. J. Phycol. 27, 21–26). J. Phycol. 28, 570–574 (1992).

Mann DG. Sexual reproduction in a marine member of the Bacillariaceae. Diatom Res. 1993;8:109–116. doi: 10.1080/0269249X.1993.9705243. DOI

Davidovich, N. A. & Bates, S. S. Patterns of sexual reproduction in the pennate diatoms Pseudo–nitzschia multiseries and P. pseudodelicatissima. In Harmful microalgae. (eds Reguera, B., Blanco, J., Fernandez, M. L., Wyatt, T.) 152–155 (Paris: Xunta de Galicia and the IOC of UNESCO, 1998).

Davidovich NA, Bates SS. Sexual reproduction in the pennate diatoms Pseudo–nitzschia multiseries and P. pseudodelicatissima (Bacillariophyceae) J. Phycol. 1998;34:126–137. doi: 10.1046/j.1529-8817.1998.340126.x. DOI

Mann, D. G. Diatoms: organism and image. In Automatic Diatom Identification. (eds du Buf, H., Bayer, M. M.) 9–40 (World Scientific Pub Co Inc., Singapore, 2002).

Sato S. Valve and girdle band morphogenesis in a bipolar centric diatom Plagiogrammopsis vanheurckii (Cymatosiraceae, Bacillariophyta) Eur. J. Phycol. 2010;45:167–176. doi: 10.1080/09670260903568483. DOI

Lobban CS, et al. Coral–reef diatoms (Bacillariophyta) from Guam: new records and preliminary checklist, with emphasis on epiphytic species from farmer–fish territories. Micronesica. 2012;43:237–479. doi: 10.1016/j.micron.2011.08.005. DOI

Mizuno M. Evolution of meiotic patterns of oogenesis and spermatogenesis in centric diatoms. Phycol. Res. 2006;54:57–64. doi: 10.1111/j.1440-1835.2006.00408.x. DOI

Mizuno M. Evolution of centric diatoms inferred from patterns of oogenesis and spermatogenesis. Phycol. Res. 2008;56:156–165. doi: 10.1111/j.1440-1835.2008.00497.x. DOI

Alverson AJ, Cannone JJ, Gutell RR, Theriot EC. The evolution of elongate shape in diatoms. J. Phycol. 2006;42:655–668. doi: 10.1111/j.1529-8817.2006.00228.x. DOI

Kaczmarska, I., Ehrman, J. M. & Bates, S. S. A review of auxospore structure, ontogeny and diatom phylogeny. In Proceedings of 16th International Diatom Symposium. (ed Economou–Amilli, A.) 153–168 (Athens: Amvrosiou, 2001).

Andersen, R. A., Berges, J. A., Harrison, P. J. & Watanabe, M. M. Recipes for freshwater and seawater media. In Algal culturing techniques (ed. Andersen, R. A.) 429–538 (Burlington, MA, 2005).

Davidovich, N. A., Davidovich, O. I. & Podunay, Y. А. The diatom culture collection at Karadag Scientific Station (Crimea). Marine Biological Journal. 2, No 1 (Morskoi Biologicheskij Zhurnal – in Russ) (2017).

Kaczmarska I, et al. Proposals for a terminology for diatom sexual reproduction, auxospores and resting stages. Diatom Res. 2013;28:263–294. doi: 10.1080/0269249X.2013.791344. DOI

Ehrman, J. M. & Kaczmarska I. Strategies for high-throughput microscopy in algal research. In: Current advances in algal taxonomy and its applications: phylogenetic, ecological and applied perspective (ed. Wołowski, K., Kaczmarska, I., Ehrman J. M. & Wojtal A. Z.) 253–262 (Kraków: W. Szafer Institute of Botany, Polish Academy of Sciences, 2012).

Doyle JJ, Doyle JL. Isolation of plant DNA from fresh tissue. Focus. 1990;12:13–15.

Daugbjerg N, Andersen RA. A molecular phylogeny of the heterokont algae based on analyses of chloroplast encoded rbcL sequence data. J. Phycol. 1997;33:1031–1041. doi: 10.1111/j.0022-3646.1997.01031.x. DOI

Jones HM, Simpson GE, Stickle AJ, Mann DG. Life history and systematics of Petroneis (Bacillariophyta) with special reference to British waters. Eur. J. Phycol. 2005;40:61–87. doi: 10.1080/09670260400024675. DOI

Boisvert S, Laviolette F, Corbeil J. Ray: simultaneous assembly of reads from a mix of high-throughput sequencing technologies. J. Comput. Biol. 2010;17:1519–1533. doi: 10.1089/cmb.2009.0238. PubMed DOI PMC

Gagnon, J. Création d’outils pour l’automatisation d’analyses phylogénétiques de génomes d’organites. M. Sc. dissertation. University of Laval (2004).

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC

Sievers F, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011;7:539. doi: 10.1038/msb.2011.75. PubMed DOI PMC

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC