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GENETIC DIVERSITY of Pyramimonas from RYUKYU ARCHIPELAGO, JAPAN (CHLOROPHYCEAE, PYRAMIMONADALES)

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GENETIC DIVERSITY of Pyramimonas from RYUKYU ARCHIPELAGO, JAPAN (CHLOROPHYCEAE, PYRAMIMONADALES) Journal of Marine Science and Technology, Vol. 21, Suppl., pp. 285-296 (2013) 285 DOI: 10.6119/JMST-013-1220-16 GENETIC DIVERSITY OF Pyramimonas FROM RYUKYU ARCHIPELAGO, JAPAN (CHLOROPHYCEAE, PYRAMIMONADALES) Shoichiro Suda1, Mohammad Azmal Hossain Bhuiyan2, 1 and Daphne Georgina Faria Key words: Pyramimonas, nuclear SSU rDNA, genetic diversity, nuclear SSU rDNA ranged from 98.2% to 99.9% and 97.3% Ryukyu Archipelago. to 98.3% within and between subgenera, respectively. The present work shows high level of genetic diversity for the genus Pyramimonas from the Ryukyu Archipelago, Japan. ABSTRACT The genus Pyramimonas Schmarda was traditionally de- I. INTRODUCTION scribed on observations of its periplast and internal structure of different flagellar apparatus or eyespot orientations and The genus Pyramimonas Schmarda was first described in currently comprises of ca. 60 species that are divided into six 1850 based on P. tetrarhynchus Schmarda a freshwater species subgenera: Pyramimonas, Vestigifera, Trichocystis, Punctatae, isolated from a ditch on Coldham’s Common, Cambridge, Hexactis, and Macrura. In order to understand the genetic United Kingdom. Subsequently, species isolated were as- diversity and phylogenetic relationships of genus Pyrami- signed to several generic names, including Pyramidomonas monas members, we analyzed nuclear SSU rDNA molecular Stein, Chloraster Ehrenberg, Asteromonas Artari, and Poly- data from 41 strains isolated from different locations of the blepharides Dangeard. The genus had shown to be artificial Ryukyu Archipelago. Phylogenetic analyses revealed that as certain freshwater species were moved to the genus Haf- strains could be segregated into six clades, four of which niomonas Ettl et Moestrup. Genus Hafniomonas resembles represented existing subgenera: Pyramimonas, Vestigifera Pyramimonas in cell shape but differs with respect to lack of McFadden, Trichocystis McFadden, and Punctatae McFadden, flagellar and body scales, different cell symmetry, flagellar root, and two undescribed subgenera. Most recovered subgenera and details of cytokinesis [18]. were represented by established and confirmed species of To date ca. sixty species have been recorded worldwide Pyramimonas along with several potentially undescribed spe- with species mostly from the marine plankton, but few benthic cies with the exception of one undescribed subgenus. Many of [9, 16, 19, 34]. The class Prasinophyceae was first formally the newly isolated strains were closely related with Pyrami- described by Moestrup and Throndsen in 1988 [20] and com- monas aurea and P. olivacea, and were considered to belong prised of unicellular green algae possessing scales on their to subgenus Punctatae. However, nuclear SSU rDNA phy- flagella and body surface. Prasinophytes (previously class logenetic trees clearly showed that they are genetically dif- Prasinophyceae) has placed great emphasis on the architecture ferent and can be divided into two subgenera. Subgenus and structure of the various scale types that are distributed on Punctatae comprised of Pyramimonas olivacea and related the flagella and cell surface [25, 27]. Hence resulting in the strains whilst, P. aurea and related strains belonged to an un- detailed study of the type species with respect to the ultra- described subgenus which is tentatively referred to as unde- structure, scale morphology and scale morphogenesis [1, 12, scribed subgenus 1 which shared a sister-group relationship 21, 31]. with subgenus Punctatae. The genetic similarity based on Early work on the genus began with light microscopy (LM) however, LM observations alone failed to assess the existing variability within species mainly because of the large degree Paper submitted 10/31/13; revised 12/15/13; accepted 12/20/13. Author for of overlap that existed with respect to cell shape, internal correspondence: Shoichiro Suda (e-mail: [email protected]). organization and dimensions [32]. Subsequently, the genus 1 Department of Chemistry, Biology and Marine Science, Faculty of Science, was emended and four subgenera were categorized based on University of the Ryukyus, Nishihara, Okinawa, Japan. electron microscopic observations [16, 17]. However, a modi- 2 Graduate School of Engineering and Science, University of the Ryukyus, Nishihara, Okinawa, Japan. fied classification of the genus at the subgeneric level was 286 Journal of Marine Science and Technology, Vol. 21, Suppl. (2013) c h 80 km g e f b 20 km a. Senagajima, Tomishiro, Okinawa b. Maeda, Onna, Okinawa c. Oku, Kunigami, Okinawa a d. Hanashiro, Yaese, Okinawa e. Abu, Nago, Okinawa f. Kayo, Nago, Okinawa d g. Seragaki, Onna, Okinawa j h. Bise, Motobu, Okinawa i. Teniya, Nago, Okinawa j. Odo, Itoman, Okinawa Fig. 1. Map of Ryukyu Archipelago, Japan (inset). Detailed sampling on Okinawa-jima Island. put forth [9] which was based on four different flagellar ap- The objective of the present study was to investigate ge- paratus or eyespot orientations and two new subgenera were netic diversity and phylogenetic relationships among Pyrami- proposed. Currently the genus is classified into the following monas species using larger taxon sampling by isolating strains six subgenera: from different locations around Ryukyu Archipelago, Japan using nuclear SSU rDNA and discuss the congruence between 1. Pyramimonas phylogeny and morphology based delineation. 2. Vestigifera McFadden 3. Trichocystis McFadden II. MATERIALS AND METHODS 4. Punctatae McFadden 5. Hexactis Hori, Moestrup & Hoffmann 1. Sampling 6. Macrura Hori, Moestrup & Hoffmann Bottom sand and water samples were collected from 15 locations throughout the Ryukyu Archipelago: Iriomote-jima Molecular phylogenetic analyses of the genus Pyramimonas Island (1), Miyako-jima Island (1), Okinawa-jima Island (10; and prasinophytes was carried out using nuclear encoded rDNA Fig. 1 for details on locations), Okinoerabu-jima Island (2), gene [18S rDNA; 6, 22, 24, 30, 35, 36], plastid encoded rDNA and Tanegashima (1). Samples were enriched with IMK gene [16S; 15], and ribulose-1, 5-biphosphate carboxylase (Nippon Pharmaceutical, Co. Tokyo, Japan) + GeO2 medium oxygenase gene [rbcL; 3, 4, 22, 30, 35]. However, relations and cultured at 24 ± 2°C under 14:10 light:dark cycle and 40 between the subgenera have remained unresolved [30]. µmol photon m-2 s-1 from cool white fluorescent tubes. The Ryukyu Archipelago located in southwestern Japan of the western Pacific Ocean consists of over 900 islands and 2. Strain Identification and Culture Establishment islets between mainland Japan and Taiwan (Fig. 1; inset) and Forty-one unialgal culture strains of typical inversely py- this region have not been investigated for the genus Pyrami- ramidal shaped flagellates were isolated by micropipetting and monas. These islands are known to sustain rich and diverse cultures were established. Table 1 lists strain names and col- flora and fauna that is mainly attributed to the Kuroshio Cur- lection information of isolated strains from Ryukyu Archi- rent and hence considered a hotspot of endemism. pelago. S. Suda et al.: Genetic Diversity of Pyramimonas 287 Table 1. List of Pyramimonas strains isolated in this study, with their strain name, geographic origin. Strain Geographic Origin Collection yy/mm/dd Longitude:Latitude 7-Py Senagajima, Itoman, Okinawa 2003/04/01 26.177N: 127.641E Te2Py Teniya, Nago, Okinawa 2003/05/01 26.565N: 128.140E Py4 Maeda, Onna, Okinawa 2004/01/22 26.444N: 127.767E Py5 Maeda, Onna, Okinawa 2004/01/22 26.444N: 127.767E Py8 Maeda, Onna, Okinawa 2004/01/22 26.444N: 127.767E Hae5Py5 Haemida, Iriomote, Taketomi, Okinawa 2004/03/07 24.271N: 123.829E Ok2P3 Oku, Kunigami, Okinawa 2004/03/23 26.849N: 128.284E M1Py1 Maeda, Onna, Okinawa 2004/04/06 26.443N: 127.768E Ab4-11 Abu, Nago, Okinawa 2004/07/02 26.538N: 128.095E Ab4-13 Abu, Nago, Okinawa 2004/07/02 26.538N: 128.095E Sa5P5 Hanashiro, Yaese, Okinawa 2004/08/30 26.115N: 127.745E Sera3-4-4 Seragaki, Onna, Okinawa 2004/09/15 26.509N: 127.864E Mad5-2 Maeda, Onna, Okinawa 2005/02/02 26.444N: 127.767E Mad 6-5 Maeda, Onna, Okinawa 2005/02/02 26.444N: 127.767E Ka5 Kayo, Nago, Okinawa 2005/03/09 26.547N: 128.108E Ka10 Kayo, Nago, Okinawa 2005/03/09 26.547N: 128.108E Ka1 Kayo, Nago, Okinawa 2005/03/09 26.547N: 128.108E Mae3P1-2 Maeda, Onna, Okinawa 2005/03/14 26.444N: 127.767E MD6-19 Maeda, Onna, Okinawa 2005/06/13 26.444N: 127.767E BiP5 Bise, Motobu, Okinawa 2005/07/22 26.710N: 127.880E Tni4Py1 Teniya, Nago, Okinawa 2005/08/07 26.565N: 128.140E Tni4Py2 Teniya, Nago, Okinawa 2005/08/07 26.565N: 128.140E Tni4Py3 Teniya, Nago, Okinawa 2005/08/07 26.565N: 128.140E Tni4Py4 Teniya, Nago, Okinawa 2005/08/07 26.565N: 128.140E MK7P4 Maeda, Onna, Okinawa 2006/03/17 26.444N: 127.767E Mk7P27 Maeda, Onna, Okinawa 2006/03/17 26.444N: 127.767E Mk7N1 Maeda, Onna, Okinawa 2006/03/17 26.444N: 127.767E MIYI-8 Aragusuku, Miyako, Okinawa 2006/06/17 24.762N: 125.426E SergOP7-2 Seragaki, Onna, Okinawa 2006/06/26 26.509N: 127.864E SergOP6-1 Seragaki, Onna, Okinawa 2006/06/26 26.509N: 127.864E SergOP9 Seragaki, Onna, Okinawa 2006/06/26 26.509N: 127.864E OEFO6-4 Furusato, Wadomari, Kagoshima 2006/07/28 27.362N: 128.626N OEF013 Furusato, Wadomari, Kagoshima 2006/07/28 27.362N: 128.626N TUP12 Urata, Nishinoomote, Kagoshima 2006/08/11 30.823N: 131.038E TU8 Urata, Nishinoomote, Kagoshima 2006/08/11 30.823N: 131.038E TU6 Urata, Nishinoomote, Kagoshima 2006/08/11 30.823N: 131.038E TU2 Urata, Nishinoomote, Kagoshima 2006/08/11 30.823N: 131.038E OD6P2 Odo, Itoman, Okinawa 2006/09/07 26.088N: 127.708E OD6P1 Odo, Itoman, Okinawa 2006/09/07 26.088N: 127.708E OEO3-3 Okidomari, Shinjyo, China, Kagoshima 2007/07/29 27.400N: 128.560N M4-1 Maeda, Onna, Okinawa 2008/05/05 26.444N: 127.767E Strain names in bold are lost. 3. DNA Extraction, Amplification, Sequencing, and quence data was aligned in BioEdit 7.0.5.3 [7]. Alignments Forty-one strains were cultured, harvested, and DNA ex- 4.
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