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Surviving the Marine Environment: Two New Species of Mallomonas (Synurophyceae) Phycologia ISSN: 0031-8884 (Print) 2330-2968 (Online) Journal homepage: https://www.tandfonline.com/loi/uphy20 Surviving the marine environment: two new species of Mallomonas (Synurophyceae) Minseok Jeong, Jong Im Kim, Bok Yeon Jo, Han Soon Kim, Peter A. Siver & Woongghi Shin To cite this article: Minseok Jeong, Jong Im Kim, Bok Yeon Jo, Han Soon Kim, Peter A. Siver & Woongghi Shin (2019): Surviving the marine environment: two new species of Mallomonas (Synurophyceae), Phycologia, DOI: 10.1080/00318884.2019.1565718 To link to this article: https://doi.org/10.1080/00318884.2019.1565718 View supplementary material Published online: 04 Apr 2019. Submit your article to this journal View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=uphy20 PHYCOLOGIA https://doi.org/10.1080/00318884.2019.1565718 Surviving the marine environment: two new species of Mallomonas (Synurophyceae) 1 1 2 3 4 1 MINSEOK JEONG ,JONG IM KIM ,BOK YEON JO ,HAN SOON KIM ,PETER A. SIVER , AND WOONGGHI SHIN 1Department of Biology, Chungnam National University, Daejeon 34134, Korea 2Nakdonggang National Institute of Biological Resources, Sangju 37242, Korea 3School of Life Science, Kyungpook National University, Daegu 41566, Korea 4Department of Botany, Connecticut College, 270 Mohegan Ave., Box 5604, New London, Connecticut 06320, USA ABSTRACT ARTICLE HISTORY The genus Mallomonas consists of single-celled flagellates covered with siliceous scales and bristles Received 19 September 2018 and is well known in freshwater environments. Two new marine Mallomonas species were collected Accepted 3 January 2019 from Dongho Beach, Jeollabukdo, Korea. To fully understand the taxonomy of the new species, we Published online 4 April 2019 performed molecular phylogenetic analysis based on a concatenated dataset and observed morpho- KEYWORDS logical features using light and electron microscopy. For the phylogenetic analysis, we used Growth rate; Mallomonas; a combined dataset from five gene sequences: nuclear small subunit (SSU) and large subunit (LSU) Marine; New species; rDNA and plastid LSU rDNA, rbcL and psaA genes. The new species M. cuspis sp. nov. grouped Phylogeny; Salinity; with M. heterospina and M. oviformis in the section Planae. It had scales with a broad shield marked Synurophyte; Ultrastructure with V-shaped internal ridge that lacked submarginal ribs and a dome. The other new species, M. marina sp. nov., clustered with M. cratis, M. pseudocratis, M. asmundiae and M. striata var. serrata in section Striatae and had scale characters that matched the group, including a well- developed posterior submarginal rib and series of transverse ribs on the shield and dome. In addition, we investigated the effect of salinity on growth rate and cell morphology. The two marine species represented high growth rate between salinities of 10 and 30 psu, suggesting that both species are well adapted in marine environments. When exposed to salinities of 0 and 5 psu, they underwent cell enlargement. INTRODUCTION large subunit (LSU) rDNA and plastid rbcLgenes(Joet al. 2013). In addition, the phylogenetic analysis of Mallomonas,basedon Mallomonas isthemostspeciosegenusintheclassSynurophyceae morphological features and moleculardata,indicatedthatitwas with about 200 taxa in 19 sections (Kristiansen 2002;Kristiansen divided into two major clades according to the presence/absence & Preisig 2007;Siver1991;Siveret al. 2015). The single-celled of a V-rib on the siliceous scales and the type of bristle produced organism has two unequal flagella and on most species only one is (Jo et al. 2011, 2013;Siveret al. 2015). emergent from the cell. The cell is covered with siliceous scales The vast majority of Mallomonas species are known from and bristles that are intricate and highly organised (Kristiansen freshwater environments worldwide, where they often form 2002;Siver1991;Siver&Glew1990). The scales are flat to slightly important components of planktic communities (Siver 1993; convex plate-like structures with a variety of designs that form the Siver & Hamer 1989). Several species included in two culture basis for inter- and infraspecies differentiation (Kristiansen 2005; strains of M. papillosa and M. cratis (see description of two Siver 1991, 2018;Siveret al. 2013). In Mallomonas, ultrastructural CCMP476 and CCMP3275 strains on the National Center for characters of scales (presence or absence of V-rib and dome, Marine Algae and Microbiota website) were previously reported secondary ornamentation) and bristles (type and position) are from freshwater to brackish environments, especially around the used to distinguish between taxa at section, series, species and Baltic Sea (Ikävalko 1994;Ikävalko&Thomsen1996;Němcová variety ranks. et al. 2016). Sampling sites in the Baltic Sea were either lakes near In an early parsimony analysis based on nuclear small subunit the shorelines or brackish waterbodies with salinities of below (SSU) rDNA and scale characteristics, the genus Mallomonas 5 psu due to freshwater inflow from both melting snow and ice formed a monophyletic lineage with the synurophycean assem- and rivers. During multiple samplings of marine sand flats at low blage Synura and Neotessella (Lavau et al. 1997). A second phylo- tide on the west coast of Korea in the winter to spring of genetic analysis using a combined nuclear SSU rDNA and plastid 2013–2017, we established cultures of two Mallomonas species rbcL sequence dataset supported monophyly of Mallomonas but with different sized cells and covered with scales and bristles. not based solely on the rbcL gene (Andersen 2007). More recently, Taxonomic studies of newly discovered Mallomonas species Mallomonas was recovered as a monophyletic assemblage among from marine environments will provide insight into species diver- synurophycean genera using a combination of nuclear SSU and sity and speciation of the photosynthetic species belonging to the CONTACT Woongghi Shin [email protected] Colour versions of one or more of the figures in the article can be found online at www.tandfonline.com/uphy. Supplemental data for this article can be accessed on the publisher’s website. © 2019 International Phycological Society 2 Phycologia Fig. 1. Bayesian tree of Mallomonas based on combined nuclear SSU and LSU rDNA and plastid LSU rDNA, rbcL and psaA sequence data. The MLBS (left) and Bayesian PP (right) are shown on each node. Scale bar indicates number of substitutions per site; thick line indicates full support (100% bootstrap value for MLBS and 1.00 for PP) and (−) denotes values < 50% for MLBS or 0.70 for PP. Jeong et al.:Survivingthemarineenvironment 3 genus Mallomonas. Here, we describe two marine were used in phylogenetic analysis; the third codon was species, M. cuspis sp. nov.andM. marina sp. nov., using light excluded due to multiple hits (Jo et al. 2011, 2013). and electron microscopy coupled with molecular data. Phylogenetic analyses MATERIAL AND METHODS A combined dataset of 9177 characters (nr SSU = 1,637, nr LSU = 2,547, pt LSU = 2,591, rbcL = 824 and psaA=1,578) Culture from 95 taxa was generated for phylogenetic analysis (Table The marine Mallomonas species (M. cuspis sp. nov. S1). Primers and ambiguously aligned regions were not used in Dongho022517B3, M. marina sp. nov. Dongho031817J) were phylogenetic analyses. The sequences of four chrysophycean collected at Dongho Beach, Jeollabukdo, Korea (35°31.00ʹN, species were used as outgroup taxa to root the tree because 126°28.97ʹE, salinity value of 28.3 psu). We performed single these taxa have been proved to be basal and have formed cell isolation using a Pasteur capillary pipette and established a sister clade with the genera Mallomonas, Synura and them as unialgal culture strains. A second strain of M. marina Neotessella in previous studies (Jo et al. 2013, 2016;Siver CCMP3275 was obtained from the National Center for et al. 2015). Maximum-likelihood (ML) phylogenetic analysis Marine Algae and Microbiota. All cultures were grown in was performed using RAxML v8.2.4 (Stamatakis 2014), with the DY-V medium (Andersen et al. 2005) with either distilled general time-reversible plus gamma (GTR + GAMMA) model. seawater or freshwater and were maintained at 17 °C using We used 1000 independent tree inferences, using the -# option a 14:10-h light:dark cycle and light intensity of c. 30 μmol of the programme to identify the best tree. Gamma correction − − photon·m 2·s 1 using cool-white fluorescent tubes (OSRAM values and the proportion of invariable sites of the combined Korea Co., Ansan, Korea). The information for each strain is dataset were obtained automatically by the programme. listed in Table S1. Maximum-likelihood bootstrap values (MLBS) were calculated using 1000 replicates with the same substitution model. Bayesian analyses were performed using MrBayes v3.2 (Ronquist et al. 2012); the best-fit model for the combined DNA extraction, amplification, sequencing and dataset was determined by the Bayesian information criterion alignment of MODELTEST v3.7 (Posada & Crandall 1998), with general The cell was harvested by centrifugation (model 5424, time-reversible plus gamma (GTR + I + G). Each analysis was Eppendorf, Hamburg, Germany) at 9391 × g for 3 min. performed using a Metropolis-coupled MarKov chain Monte Genomic DNA was extracted using a DOKDO-Prep Blood Carlo approach, with 2,000,000 cycles for each chain. Trees Genomic DNA Purification Kit (ELPIS-Biotech Inc., Daejeon, were saved to a file
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