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Dwelling Dinoflagellate Genus, Pachena (Dinophyceae), with Descriptions of Three New Species 1

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Dwelling Dinoflagellate Genus, Pachena (Dinophyceae), with Descriptions of Three New Species 1 J. Phycol. 56, 798–817 (2020) © 2020 The Authors. Journal of Phycology published by Wiley Periodicals, Inc. on behalf of Phycological Society of America This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. DOI: 10.1111/jpy.12984 MORPHOLOGY AND MOLECULAR PHYLOGENY OF A NEW MARINE, SAND-DWELLING DINOFLAGELLATE GENUS, PACHENA (DINOPHYCEAE), WITH DESCRIPTIONS OF THREE NEW SPECIES 1 Mona Hoppenrath 2 Senckenberg am Meer, German Centre for Marine Biodiversity Research (DZMB), S udstrand€ 44, Wilhelmshaven D – 26382, Germany Albert Re n~e Departament de Biologia Marina i Oceanografia, Institut de Ci encies del Mar (CSIC), Pg. Mar ıtim de la Barceloneta, 37-49, Barcelona, Catalonia 08003, Spain Cecilia Teodora Satta Dipartimento di Architettura, Design e Urbanistica, University of Sassari, Via Piandanna 4, Sassari 07100, Italy Agenzia Ricerca per l’Agricoltura (AGRIS), Loc Bonassai, Olmedo, Sassari 07100, Italy Aika Yamaguchi Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan and Brian S. Leander The Departments of Botany and Zoology, University of British Columbia, 6270 University Boulevard, Vancouver BC V6T 1Z4, Canada Marine benthic dinoflagellates are interesting not based on SSU and LSU rDNA sequences contribute only because some epiphytic genera can cause to understanding the evolution of the planktonic harmful algal blooms but also for understanding relatives of Pachena , the Thoracosphaeraceae. dinoflagellate evolution and diversification. Our Key index words: benthic; distribution; morphology; understanding of their biodiversity is far from Peridiniales; protists; taxonomy; Thoracosphaer- complete, and many thecate genera have unusual aceae tabulatio n patterns that are difficult to relate to the diverse known phytoplankton taxa. A new sand- Abbreviations : AICc, corrected Akaike information dwelling genus, Pachena gen. nov., is described based criterion; APC, apical pore complex; (B)PP, (Baye- on morphological and DNA sequence data. Three sian) posterior probability; BS, bootstrap; DIC, species were discovered in distant locations and are differential interference contrast; HMDS, hexam- circumscribed, namely, P. leibnizii sp. nov. from ethyldisilazane; ML, maximum likelihood; Po, apical Canada, P. abriliae sp. nov. from Spain, and P. pore plate; 1 0, first apical plate; 2 0, second apical plate; meriddae sp. nov. from Italy. All species are tiny 30, third apical plate; 4 0, forth apical plate; 1a, first (about 9 –23 lm long) and heterotrophic. Species are intercalary plate; 2a, second intercalary plate; 3a, third characterized by their tabulation (APC 4 0 3a 6 00 5c 5s intercalary plate; 1 00 , first precingular plate; 2 00 , second 5000 20000 ), an apical hook covering the apical pore, an precingular plate; 3 00 , third precingular plate; 4 00 , ascending cingulum, and a sulcus with central list. fourth precingular plate; 5 00 , fifth precingular plate; The first anterior intercalary plate is uniquely 600 , sixth precingular plate; c1, first cingular plate; c2, “sandwiched” between two plates. The species share second cingular plate; c3, third cingular plate; c4, these features and differ in the relative sizes and fourth cingular plate; c5, fifth cingular plate; Sa, ante- arrangements of their plates, especially on the rior sulcal plate; Sd, right sulcal plate; Ss, left sulcal epitheca. The ornamentation of thecal plates is plate; Sp, posterior sulcal plate; Sm, median sulcal species-specific. The new molecular phylogenies plate; 1 000 , first postcingular plate; 2 000 , second postcin- gular plate; 3 000 , third postcingular plate; 4 000 , fourth 1 Received 11 December 2019. Accepted 14 February 2020. First postcingular plate; 5 000 , fifth postcingular plate; 1 0000 , Published Online 6 March 2020. Published Online 2 April 2020, first antapical plate; 2 0000 , second antapical plate Wiley Online Library (wileyonlinelibrary.com). 2Author for correspondence: e-mail: mhoppenrath@sencken berg.de. Editorial Responsibility: C. Lane (Associate Editor) 798 DESCRIPTION OF PACHENA GEN. NOV. 799 The first studies on sand-dwelling dinoflagellates Studies on benthic dinoflagellates from the Mediter- were conducted in the early twentieth century ranean Sea have mainly focused on epiphytic toxic (Kofoid and Swezy 1921, Herdman 1922, 1924a,b, species (Vila et al. 2001, Aligizaki and Nikolaidis Balech 1956), even though they were not studied 2006, Aligizaki et al. 2009, Penna et al. 2012), comprehensively until the 2000s (Hoppenrath whereas sand-dwelling dinoflagellates have been 2000a, Murray 2003, Tamura 2005, Mohammad- poorly studied and information is scarce (Re n~e Noor et al. 2007, Al-Yamani and Saburova 2010). et al. 2020). Here, a new genus is described that was The studies showed that the species composition is first discovered on the western shoreline of Vancou- distinct from planktonic communities and the spe- ver Island, Canada and further species were cies diversity was largely unexplored (Hoppenrath recorded in Spanish and Italian Mediterranean Sea et al. 2014). Epiphytic species have received more samples. attention from the scientific community, mainly because many of them are toxin producers and are METHODS toxic to humans (Berdalet et al. 2017). Still there is undiscovered biodiversity among benthic, especially Sampling, cell extractions, and microscopy . Sand samples from sand-dwelling, dinoflagellates with new taxon Canada were collected with a spoon during low tide at Pachena Beach (48 °47 034.6 ″ N, 125 °07 019.0 ″ W), Vancou- descriptions nearly every year, including new gen- ver Island, British Columbia, in May and June 2005, April era: Vulcanodinium (N ezan and Chom erat 2011), and June 2006, and May and June 2007. The sand sam- Moestrupia (Hansen and Daugbjerg 2011), Ankistro- ples were transported directly to the laboratory, and dinium (Hoppenrath et al. 2012), Testudodinium dinoflagellates were separated from the sand by extraction (Horiguchi et al. 2012), Bispinodinium (Yamada through a fine filter (mesh size 45 lm) using melting sea- et al. 2013), Ailadinium (Saburova and Chom erat water ice (Uhlig 1964). Cells of the new taxon were observed directly with a Leica DMIL inverted microscope 2014), Madanidinium (Chom erat and Bilien 2014), (Wetzlar, Germany) and isolated by micropipetting for Aduncodinium (Kang et al. 2015), Fukuyoa (G omez the preparations described below. For differential interfer- et al. 2015), Pellucidodinium (Onuma et al. 2015), ence contrast (DIC) light microscopy, pipetted cells were Laciniporus (Saburova and Chom erat 2019), and viewed with a Zeiss Axioplan 2 imaging microscope (Carl- Psammodinium (Re n~e and Hoppenrath 2019). Zeiss, Oberkochen, Germany) connected to a Leica Benthic, sand-dwelling species seem to have mor- DC500 color digital camera. phological adaptations reflecting their life in the Mediterranean sediment samples from the Catalan Coast ° ″ interstitial habitat, such as smooth (i.e., without strik- were obtained at Castelldefels Beach (41 15 037.0 N; 1°55 048.8 ″ E) during spring and summer months from 2015 ing extensions like wings, spines, or horns) and flat- to 2017. Sediment samples from Sardinian beaches were tened cell shapes (Hoppenrath et al. 2014). Several obtained at Platamona Beach (40 °49 027.1 ″ N; 8 °31 036.4 ″ E) taxa cover their apical pore with thecal extensions and La Speranza Beach (40 °29 043.1 ″ N; 8 °22 012.1 ″ E) during (e.g., Rhinodinium has a large apical hook; Murray summer months in 2015 and 2018. Surface samples were et al. 2006); some Amphidiniopsis species and Herdma- taken by snorkeling at a depth of approximately 1.5 –2 m with nia have a small hook (Hoppenrath 2000b, Murray plastic bottles. The distance to the shore depended on the underwater slope of each beach. The sediments were kept at and Patterson 2002, Toriumi et al. 2002, Yamaguchi room temperature, in the dark, and immediately taken to the et al. 2011, Re n~e et al. 2020); Apicoporus has finger- laboratory. Once there, cells were extracted from the sedi- like projections (Sparmann et al. 2008); Laciniporus ment using the melting seawater-ice method (Uhlig 1964). has a small flap-shaped projection (Saburova and Subsamples were fixed with Lugol’s iodine or formaldehyde Chom erat 2019); and Sinophysis has parallel upright (2%) and preserved in the dark at 4 °C. Alive and fixed sam- projections (Hoppenrath 2000c, Chom erat 2016). ples from the Catalan coast were observed under a phase-con- trast Leica DM-IRB inverted microscope (Leica Microsystems, Many thecate, benthic dinoflagellate taxa have unu- Wetzlar, Germany) connected to a ProgRes C10 (Jenoptik sual tabulation patterns that are difficult to relate to Laser, Optik Systeme GmbH, Jena, Germany) digital camera. the known tabulations in planktonic taxa (Hoppen- Cell measurements were conducted using the ProgRes Cap- rath et al. 2014). For example, Madanidinium has no turePro software (Jenoptik Laser; Optik Systeme GmbH). Live apical pore (Chom erat and Bilien 2014); Plagiodinium samples from the Sardinian coast were observed under a Zeiss has no precingular or no apical plate series (Faust 100 inverted microscope (Carl Zeiss, Oberkochen, Germany), equipped with DIC. Digital photos were taken using a Zeiss and Balech 1993, Wakeman et al. 2018), depending Axiocam (Carl Zeiss). Cell measurements were obtained from on interpretation; Thecadinium sensu stricto and Pseu- LM and SEM images using the ImageJ
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