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(Mamiellales, Mamiellophyceae), Two New Green Algal Species from the High Arctic1

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(Mamiellales, Mamiellophyceae), Two New Green Algal Species from the High Arctic1 J. Phycol. 56, 37–51 (2020) © 2019 Phycological Society of America DOI: 10.1111/jpy.12932 MANTONIELLA BEAUFORTII AND MANTONIELLA BAFFINENSIS SP. NOV. (MAMIELLALES, MAMIELLOPHYCEAE), TWO NEW GREEN ALGAL SPECIES FROM THE HIGH ARCTIC1 Sheree Yau2,3 Integrative Marine Biology Laboratory (BIOM), CNRS, UMR7232, Sorbonne Universite, Banyuls sur Mer, France Adriana Lopes dos Santos Asian School of the Environment, Nanyang Technological University, 50 Nanyang Avenue, Singapore, Singapore Centro de Genomica, Ecologıa y Medio Ambiente, Facultad de Ciencias, Universidad Mayor, Camino La Piramide 5750, Huechuraba, Santiago, Chile Wenche Eikrem Norwegian Institute for Water Research, Gaustadalleen 21, 0349, Oslo, Norway Department of Biosciences, University of Oslo, P.O. box 1066, Blindern, Oslo 0316, Norway Natural History Museum, University of Oslo, P.O. box 1172 Blindern 0318, Oslo, Norway Catherine Gerikas Ribeiro , Priscillia Gourvil Sorbonne Universite, CNRS, UMR7144, Station Biologique de Roscoff, Roscoff, France Sergio Balzano Stazione Zoologica Anton Dohrn, Istituto Nazionale di Biologia, Ecologia e Biotecnologie Marine, Naples, Italy Marie-Line Escande, Herve Moreau Integrative Marine Biology Laboratory (BIOM), CNRS, UMR7232, Sorbonne Universite, Banyuls sur Mer, France and Daniel Vaulot Sorbonne Universite, CNRS, UMR7144, Station Biologique de Roscoff, Roscoff, France Asian School of the Environment, Nanyang Technological University, 50 Nanyang Avenue, Singapore, Singapore Members of the class Mamiellophyceae comprise M. beaufortii and M. baffinensis are most similar to the species that can dominate picophytoplankton cosmopolitan M. squamata with only minor dif- diversity in polar waters. Yet, polar species are often ferences in scale structure distinguishing them. morphologically indistinguishable from temperate Screening of global marine metabarcoding data sets species, although clearly separated by molecular indicates M. beaufortii has only been recorded in features. Here we examine four Mamiellophyceae seawater and sea ice samples from the Arctic, while strains from the Canadian Arctic. The 18S rRNA and no environmental barcode matches M. baffinensis. Internal Transcribed Spacer 2 (ITS2) gene phylogeny Like other Mamiellophyceae genera that have distinct place these strains within the family Mamiellaceae polar and temperate species, the polar distribution of (Mamiellales, Mamiellophyceae) in two separate these new species suggests they are cold or ice- clades of the genus Mantoniella. ITS2 synapo- adapted Mantoniella species. morphies support their placement as two new Key index words: Arctic; ITS; Mamiellophyceae; species, Mantoniella beaufortii and Mantoniella Mantoniella;metabarcoding;picophytoplankton;polar baffinensis. Both species have round green cells with diameter between 3 and 5 lm, one long flagellum and Abbreviations: CBC, compensatory base change; a short flagellum (~1 lm) and are covered by hCBC, hemi-CBC; AIC, Akaike information criterion; spiderweb-like scales, making both species similar to BIC, Bayesian information criterion; DIC, differential Mantoniella other species. Morphologically, interference contrast; HPLC, high-performance liquid chromatography; ITS, Internal Transcribed Spacer; 1 Received 22 December 2018. Accepted 22 July 2019. First Pub- OSD, Ocean Sampling Day; PTFE, Polytetrafluor- lished Online 14 October 2019. Published Online 17 November 2019, Wiley Online Library (wileyonlinelibrary.com). oethylene; SPR, Subtree Pruning and Regrafting; 2 Present address: Department of Marine Biology and Oceanogra- TEM, Transmission electron microscopy phy, Institute of Marine Sciences (ICM), CSIC, Barcelona Spain. 3Author for correspondence: e-mail [email protected]. Editorial Responsibility: B. Palenik (Associate Editor) 37 38 SHEREE YAU ET AL. Over the last few decades, the taxonomy of green species M. polaris, and species originating from algae has gone through a profound reorganization. lower latitudes as M. bravo, M. commoda, and The class Prasinophyceae, initially defined as scaly M. pusilla (Simon et al. 2017). Similarly, in Man- flagellates (Moestrup and Throndsen 1988), has toniella, M. antarctica was described from the Antarc- been rearranged into several new classes including tic, whereas M. squamata was cosmopolitan Chlorodendrophyceae, Chloropicophyceae, and (Marchant et al. 1989). Mamiellophyceae (Massjuk 2006, Marin and Melko- Three picophytoplanktonic strains (RCC2285, nian 2010, Lopes dos Santos et al. 2017b), as well as RCC2288, and RCC2497) were isolated in the Cana- clades without formal names (Guillou et al. 2004, dian Arctic from mesophilic surface water sampled Tragin et al. 2016), leading to the abandonment of at two sites in the Beaufort Sea in the summer of the class name Prasinophyceae. The Mamiel- 2009 as part of the MALINA cruise (Balzano et al. lophyceae are ecologically successful and particu- 2012). A fourth strain (RCC5418) was subsequently larly dominant in marine coastal waters (Lopes dos isolated from sea ice collected in Baffin Bay in the Santos et al. 2017a, Tragin and Vaulot 2018). The spring as part of the Green Edge project. We per- first scaled species of Mamiellophyceae observed formed a combination of molecular, morphological, were Mantoniella squamata (as Micromonas squamata, and pigment characterization of these isolates, Manton and Parke 1960) and Mamiella gilva (as which we propose to constitute two novel Man- Nephroselmis gilva; Park and Rayns 1964). Moestrup toniella species, M. beaufortii and M. baffinensis, (1984) erected the family Mamiellaceae, which restricted to polar environments. included Mantoniella and Mamiella, with Mamiella gilva designated as the type species. Mamiel- lophyceae comprises three orders: Monomastigales, METHODS with one freshwater genus Monomastix; Doli- Culture conditions. Strains RCC2285, RCC2288, and chomastigales, with two genera Crustomastix and RCC2497 were isolated from seawater collected at two sites Dolichomastix; and Mamiellales, which currently com- (70°300 N, 135°300 W and 70°340 N, 145°240 W) in the Beau- prises five genera Bathycoccus, Mamiella, Mantoniella, fort Sea in the summer of 2009 as part of the MALINA cruise Micromonas, and Ostreococcus. As these genera are as described previously (Balzano et al. 2012). Strain RCC5418 morphologically heterogeneous, with Micromonas was isolated from the Green Edge project Ice Camp (http:// www.greenedgeproject.info/), a sampling site on the sea ice and Ostreococcus lacking scales and Bathycoccus and near the village of Qikiqtarjuaq (67°28.7840 N, 63°47.3720 W). Ostreococcus lacking flagella, the monophyly of Sampling was conducted between April 20 and July 27, 2016, Mamiellophyceae was established based on nuclear beginning in completely snow covered conditions followed by and plastid rRNA sequence and secondary structure bare ice and ending when the ice was broken out. Sea ice from May 23, 2016 was melted overnight and 200 mL was analyses (Marin and Melkonian 2010). l Molecular analyses of the Mamiellophyceae have gravity filtered (Sartorius filtration system) through 3 m pore size polycarbonate filters (Millipore Isopore membrane, permitted the description of otherwise morphologi- 47 mm). 500 lL of filtrate was enriched by addition to 15 mL cally indistinguishable cryptic species. For example, of L1 medium (NCMA, Bigelow Laboratory for Ocean wide genetic diversity has been shown to exist Sciences, ME, USA). The enrichment culture was purified by dilution to 10 cells per well in a 96-deep-well plate (Eppen- between morphologically identical Ostreococcus spe- À À cies where less than 1% difference in the 18S rRNA dorf) and incubated under white light (100 lE Á m 2 Á s 1) ° gene corresponds to up to 30% of variation in in a 12:12 h light:dark cycle at 4 C. Cell growth was observed by the development of coloration after a few weeks. Culture orthologous protein coding sequences (Palenik purity was assessed by flow cytometry (Becton Dickinson, et al. 2007, Piganeau et al. 2011). From an early Accuri C6). After confirmation of the purity, the culture was stage, 18S rRNA-defined clades of Micromonas and transferred in a 50 mL ventilated flask (Sarstedt). Cultures Ostreococcus were observed to have distinct geo- are maintained in the Roscoff Culture Collection (http:// graphic distributions, suggesting their genetic varia- roscoff-culture-collection.org/) in K/2 (Keller et al. 1987) or L1 medium at 4°C under a 12:12 h light: dark cycle at 100 tion reflected adaptations to ecological niches l (Rodrıguez et al. 2005, Foulon et al. 2008) and that E light intensity. RCC2285 has been lost from culture since molecular analyses (described below) were performed. For these clades represented distinct species. Ostreococcus pigment analysis and electron microscopy, RCC2288 was is divided into rare species restricted to estuarine grown at 7°C under continuous light at 100 lE intensity in (O. mediterraneus) and coastal environments L1 medium prepared using autoclaved seawater from off- (O. tauri), as well as more abundant oceanic species shore Mediterranean Sea water diluted 10% with MilliQ water (O. lucimarinus and clade B; Demir-Hilton et al. and filtered prior to use through 0.22 lm filters. Holotype 2011, Treusch et al. 2012, Hu et al. 2016, Simmons specimens were deposited in O (Natural History Museum, University of Oslo), herbarium acronym follows Thiers et al. 2016). Micromonas cells were observed to be (2019). abundant in the Arctic Ocean (Throndsen and Kris- Sequences. Nuclear 18S rRNA and the Internal
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