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Taxonomy and Phylogeny of the Genus Cryptomonas (Cryptophyceae, Cryptophyta) from Korea

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Taxonomy and Phylogeny of the Genus Cryptomonas (Cryptophyceae, Cryptophyta) from Korea Research Article Algae 2013, 28(4): 307-330 http://dx.doi.org/10.4490/algae.2013.28.4.307 Open Access Taxonomy and phylogeny of the genus Cryptomonas (Cryptophyceae, Cryptophyta) from Korea Bomi Choi1, Misun Son2, Jong Im Kim1 and Woongghi Shin1,* 1Department of Biology, Chungnam National University, Daejeon 305-764, Korea 2Yeongsan River Environment Research Center, Gwangju 500-480, Korea The genus Cryptomonas is easily recognized by having two flagella, green brownish color, and a swaying behavior. They have relatively simple morphology, and limited diagnostic characters, which present a major difficulty in differen- tiating between species of the genus. To understand species delineation and phylogenetic relationships among Crypto- monas species, the nuclear-encoded internal transcribed spacer 2 (ITS2), partial large subunit (LSU) and small subunit ribosomal DNA (rDNA), and chloroplast-encoded psbA and LSU rDNA sequences were determined and used for phylo- genetic analyses, using Bayesian and maximum likelihood methods. In addition, nuclear-encoded ITS2 sequences were predicted to secondary structures, and were used to determine nine species and four unidentified species from 47 strains. Sequences of helix І, ІІ, and ІІІb in ITS2 secondary structure were very useful for the identification of Cryptomonas spe- cies. However, the helix ІV was the most variable region across species in alignment. The phylogenetic tree showed that fourteen species were monophyletic. However, some strains of C. obovata had chloroplasts with pyrenoid while others were without pyrenoid, which used as a key character in few species. Therefore, classification systems depending solely on morphological characters are inadequate, and require the use of molecular data. Key Words: Cryptomonas; Cryptophyta; morphology; phylogeny; taxonomy INTRODUCTION The genus Cryptomonas, which belongs to the class display one or two morphotypes within a clonal culture. Cryptophyceae, was established by Ehrenberg (1831). It is In the cryptomorph, the inner periplast component (IPC) distributed in freshwater habitats worldwide. Cells can be is made of hexagonal to polygonal plates, whereas in the easily recognized by two unequal biflagella, olive-brown- camphylomorph the IPC is a sheet-like layer (Faust 1974, ish to olive-greenish in color, large ejectisomes lined in Brett and Wetherbee 1986, Hill 1991, Hoef-Emden and the furrow-gullet system, and a peculiar swaying swim- Melkonian 2003, Hoef-Emden 2007). ming behavior due to the asymmetric shape, dorsally flat- Since Ehrenberg (1831, 1832) described six Crypto- tened and ventrally concave in lateral view. Cells have two monas species, many additional species were added chloroplasts originated from red algae, which contain the (Pascher 1913, Schiller 1925, 1929, 1957, Skuja 1939, 1948, accessory pigment phycoerythrin 566 of phycobiliprotein 1956, Huber-Pestalozzi 1950, Starmach 1974). Tradition- (Hill and Rowan 1989, Clay et al. 1999, Deane et al. 2002, ally, Cryptomonas species have been characterized by Hoef-Emden and Melkonian 2003). Cryptomonas species mainly morphological characters, such as cell size, cell This is an Open Access article distributed under the terms of the Received August 20, 2013, Accepted December 5, 2013 Creative Commons Attribution Non-Commercial License (http://cre- Corresponding Author ativecommons.org/licenses/by-nc/3.0/) which permits unrestricted * non-commercial use, distribution, and reproduction in any medium, E-mail: [email protected] provided the original work is properly cited. Tel: +82-42-821-6409, Fax: +82-42-822-9690 Copyright © The Korean Society of Phycology 307 http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860 Algae 2013, 28(4): 307-330 onymized both genera Campylomonas and Chilomonas to the genus Cryptomonas. More recently, Hoef-Emden (2007) revised the genus Cryptomonas again, and pro- vided a secondary structure of the nuclear internal tran- scribed spacer 2 (ITS2) as a good marker to identify Cryp- tomonas species. In addition, she emended five species based on molecular signatures as diagnostic characters. In this study, we report unrecorded Korean Cryptomo- nas species isolated from freshwaters. We infer phylo- genetic relationships among species using a combined nuclear-encoded ITS2, partial large subunit ribosomal DNA (LSU rDNA), and small subunit ribosomal DNA (SSU rDNA), and chloroplast-encoded psbA (photosys- tem II protein D1) and LSU rDNA sequence data. We also predicted the ITS2 secondary structure of Cryptomonas Fig. 1. Distributions of the genus Cryptomonas species from Korea. species. MATERIALS AND METHODS shape, and internal organization (Bourelly 1970). Howev- er, it is difficult to delimit Cryptomonas species due to the Algal cultures and microscopy paucity of morphological characters and the less-than- adequate visibility of living cells using light microscopy Specimens were collected from freshwater habitats in (Pringsheim 1968). For example, an early attempt to orga- Korea (Fig. 1). Live cells were isolated by Pasteur capillary nize photosynthetic cryptomonad taxonomy was carried pipette and were brought into a unialgal culture. The cells out by Ehrenberg (1838), who included several unrelated were cultivated in f/2 medium (Guillard and Ryther 1962, genera in the family Cryptomonadina with original short Guillard 1975) with soil extract. The clonal cultures were diagnosis. Later, Dujardin (1841) described two families maintained under a light : dark regime of 14 : 10 at 20- (Xanthodiscaceae and Chilomonaceae) within the or- 22°C using cool-white fluorescence lamps with illumina- der Cryptomonadineae. In his classification system, the tions of 30 µmol protons m-2 s-1. The morphology was ex- family Chilomonadaceae consisted of four genera (Chi- amined by differential interference contrast with a 100X lomonas, Rhodomonas, Cryptomonas, and Cyanomonas). oil immersion lens (Carl Zeiss Co., Göttingen, Germany). These genera were characterized by nutritional mode, Calibration of magnification was done with grated mi- number and color of chloroplast. Butcher (1967) orga- crometer. The shape and length of cells, length of the nized main photosynthetic genera of the Cryptophyceae fullow-gullet system, color and number of chloroplasts, into three families (Hilleaceae, Hemiselmidaceae, and presence / absence and number of pyrenoids were exam- Cryptomonadaceae) based on complexity of furrow- ined. Cellular dimensions were determined by measuring gullet system with or without ejectisome. He also used 20-25 cells of each taxon from photographic images. Light number of ejectisome rows in the furrow-gullet system to micrographs were taken with an Axio CamHRc (Carl Zeiss discriminate between each genus, and thus, described 12 Co.) photomicrographic system attached to the micro- new Cryptomonas species from salt water. scope. Hill (1991) revised the broad generic definition of the genus Cryptomonas recognized by Butcher (1967) and DNA isolation, polymerase chain reaction (PCR), erected four new genera based on their furrow-gullet and sequencing system, periplast structure, plastidial complex and rhi- zostyle; Campylomonas, Geminigera, Storeatula, and Approximately 10 mL of cultures in exponential growth Teleaulax. Recently, molecular work (Marin et al. 1998, were harvested by centrifugation (4,500 ×g, model 5415; Deane et al. 2002) has shown that Cryptomonas species Eppendorf, Hamburg, Germany) for 1 min at room tem- grouped together with species of Campylomonas and perature and washed three times with sterilized distilled Chilomonas. Hoef-Emden and Melkonian (2003) syn- water. Total genomic DNA was extracted from the pellet http://dx.doi.org/10.4490/algae.2013.28.4.307 308 Choi et al. Taxonomy of the Genus Cryptomonas using the Dokdo-Prep Blood Genomic DNA Purification The alignment for each gene sequence was aligned by the Kit (Elpis-Biotech Inc., Daejeon, Korea) following the eye, and was edited using the Genetic Data Environment manufacturer’s blood sample protocol. PCR was per- (GDE 2.4) program (Smith et al. 1994). Unalignable nucle- formed using specific primers for nuclear ITS2, nuclear otides were excluded from phylogenetic analyses. SSU rDNA, chloroplast psbA and chloroplast LSU rDNA (Table 1). The PCR amplification was performed on a to- Strain identification tal volume of 25 µL, containing 0.15 µL of TaKaRa Ex Taq DNA polymerase (TaKaRa Bio Inc., Otsu, Japan), 2 µL Nuclear ITS2 is likely a suitable marker to identify spe- of each dNTP, 2.5 µL of 10× Ex Taq buffer, 1 µL of each cies according to its degree of conservation (Hoef-Emden primer, and 1-10 ng of template DNA. The nuclear ITS2, 2007), and nuclear ITS2 as well as partial LSU rDNA se- nuclear SSU rDNA, chloroplast psbA, and chloroplast quences were used to examine groups of genetically iden- LSU rDNA were amplified using a PTC-0150 Minicycler tical strains and to identify species of the strains. (MJ Research, Perkin-Elmer Co., Norwalk, CT, USA) with the following program: 94°C for 5 min, 30 cycles of 94°C Phylogenetic analyses for 1 min, 37-55°C for 1 min, and 72°C for 4 min, 72°C for 10 min and a 4°C hold. The PCR products were ~1.5 kb Phylogenetic trees were constructed using Bayesian for nr ITS2 partial LSU rDNA, 1.7 kb for nr SSU rDNA, 1.0 analysis (BA). Before the BA, we performed a likelihood kb for cp psbA, and 2.7 kb for cp LSU rDNA and were pu- ratio test using Modeltest, version 3.7 (Posada and Cran- rified using the Dokdo-Prep PCR Purification Kit (Elpis- dall 1998) to determine the best model
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