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Phylogeny and Morphology of a Chattonella (Raphidophyceae) Species from the Mediterranean Sea: What Is C

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Phylogeny and Morphology of a Chattonella (Raphidophyceae) Species from the Mediterranean Sea: What Is C This article was downloaded by: [Stiftung Alfred Wegener Institute für Polar- und Meeresforschung ] On: 17 April 2013, At: 02:13 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK European Journal of Phycology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tejp20 Phylogeny and morphology of a Chattonella (Raphidophyceae) species from the Mediterranean Sea: what is C. subsalsa? Sascha Klöpper a , Uwe John a , Adriana Zingone b , Olga Mangoni c , Wiebe H.C.F. Kooistra b & Allan D. Cembella a a Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570, Bremerhaven, Germany b Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Naples, Italy c Department of Biological Sciences, University Federico II, Via Mezzocannone 8, 80138, Naples, Italy Version of record first published: 13 Mar 2013. To cite this article: Sascha Klöpper , Uwe John , Adriana Zingone , Olga Mangoni , Wiebe H.C.F. Kooistra & Allan D. Cembella (2013): Phylogeny and morphology of a Chattonella (Raphidophyceae) species from the Mediterranean Sea: what is C. subsalsa?, European Journal of Phycology, 48:1, 79-92 To link to this article: http://dx.doi.org/10.1080/09670262.2013.771412 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Eur. J. Phycol. (2013), 48(1):79–92 Phylogeny and morphology of a Chattonella (Raphidophyceae) species from the Mediterranean Sea: what is C. subsalsa? SASCHA KLÖPPER1, UWE JOHN1, ADRIANA ZINGONE2, OLGA MANGONI3, WIEBE H.C.F. KOOISTRA2 AND ALLAN D. CEMBELLA1 1Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany 2Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy 3Department of Biological Sciences, University Federico II, Via Mezzocannone 8, 80138 Naples, Italy (Received 4 July 2012; revised 19 October 2012; accepted 29 October 2012) We analysed the molecular and morphological features of strains of Chattonella subsalsa isolated from the western Adriatic coast (Mediterranean Sea), with the aim of confirming their classification and elucidating their phylogenetic positions within the Raphidophyceae. We sequenced parts of the ribosomal operon, including the small subunit (SSU), the internal transcribed spacer region (ITS) and the large subunit (LSU) of the rDNA. Additionally, we analysed sequences of the chloroplast-encoded subunit psaA of Photosystem I (PSI) and rbcL, encoding the large subunit of the Rubisco gene. For three phylogenetic markers (LSU, ITS, rbcL), the sequences of the strains from the Adriatic Sea were identical and for two markers (SSU, psaA) only minor differences occurred. All strains were sister to, but well separated from, sequences from isolates in culture collections and from GenBank, thus far classified as belonging to C. subsalsa. Light and electron microscopy provided evidence for morphological differences between a strain of C. subsalsa (CCMP217) from the Gulf of Mexico and the isolates from the Adriatic Sea. Differences concerned the shape and arrangement of chloroplasts and the presence of mucocysts and other surface microstructures, which were only observed in isolates from the Adriatic Sea. This is the first evidence for two different taxa classified as C. subsalsa, which are clearly separated on the basis of several genetic markers and also show morphological differences. As compared with strains assigned to C. subsalsa from the NCMA (formerly CCMP) culture collection, the Adriatic strains more closely match the original species description. This would imply that strain CCMP217 and other genetically similar strains should be described under a new species name. Nevertheless, given the high morphological plasticity of Chattonella species, the definition of the true C. subsalsa must be decided based on detailed morphological and molecular analysis of more strains from other geographical areas. Key words: Chattonella subsalsa; compensatory base changes; harmful algae; Mediterranean Sea; molecular phylogeny; morphology; psaA; Raphidophyceae; rbcL; rDNA Introduction heterodynamic flagella emerging from a groove at the anterior end of the cell. A flagellum covered with The Raphidophyceae (described by Chadefaud, 1950, tripartite hairs is directed forward and pulls the cell, and emended by Silva, 1980) are classified within the while a flagellum with no hairs trails backwards. Cells stramenopiles, together with other prominent protists, of several species contain a variable number of ejecto- such as diatoms and chrysophytes. In a recent evolu- somes, which take the form of easily discharged Downloaded by [Stiftung Alfred Wegener Institute für Polar- und Meeresforschung ] at 02:13 17 April 2013 tionary tree of eukaryotes (Keeling et al., 2005), the mucocysts. Numerous chloroplasts are densely stramenopiles are placed with the alveolates (includ- packed in the periphery of the cell, just below the ing dinoflagellates and ciliates) within the chromal- surface, and vary in colour from green to yellow- veolates, as one of the five ‘supergroups’ identified in green to golden brown. Marine raphidophytes contain this system. Alternatively, six groups are proposed in chlorophyll a, c and/or c , and diadinoxanthin, fucox- the classification by Adl et al. (2005), who also con- 1 2 anthin and violaxanthin as the major carotenoids. sider with caution the grouping of stramenopiles with There are also pigment variants, which can be alveolates. restricted to particular genera; for example, Members of the class Raphidophyceae are unicel- Fibrocapsa and Haramonas species differ in the pre- lular, naked flagellates, which swim by means of two sence of fucoxanthinol in Fibrocapsa but 19-butanoy- loxyfucoxanthin in Haramonas (Bjørnland & Liaaen- Correspondence to: Uwe John. E-mail: [email protected] Jensen, 1989; Mostaert et al., 1998). ISSN 0967-0262 (print)/ISSN 1469-4433 (online)/13/010079-92 © 2013 British Phycological Society http://dx.doi.org/10.1080/09670262.2013.771412 S. Klöpper et al. 80 Eleven marine raphidophyte species have been particularly problematic. Chattonella marina, C. anti- described within six genera (Chattonella, Fibrocapsa, qua and C. ovata were first described based upon Haramonas, Heterosigma, Chlorinimonas and morphological characters visible by light microscopy, Viridilobus), the latest addition being Viridilobus mar- but they were subsequently shown to exhibit high inus (Demir-Hilton et al., 2012). Among these raphi- sequence similarities for different genetic markers dophytes, seven species have been associated with fish (Hirashita et al., 2000; Bowers et al., 2006; Hosoi- kills (Hallegraeff et al., 1998). There is no evidence of Tanabe et al., 2006; Demura et al., 2009). Based on harmful effects caused by the three known Haramonas the most recent molecular and morphological find- species or by Chlorinimonas sublosa, perhaps because ings, it has been suggested that differences among their sand-dwelling habit limits contact with fish these three taxa warrant them to be accorded at most shoals. Several harmful events have been caused by varietal status (Demura et al., 2009), the valid name species in the genus Chattonella, including the subject for the species being C. marina (Subrahmanyan) Y. of the present paper, C. subsalsa (Imai & Yamaguchi, Hara & Chihara , which comprises C. var. marina, var. 2012). The monotypic genus Heterosigma and the antiqua (Hada) Demura & Kawachi, and var. ovata genus Fibrocapsa, containing F. japonica and a (Y. Hara & Chihara) Demura & Kawachi. In the recently described new genotype from the phylogenetic trees presented in the publications men- Mediterranean (Klöpper et al., 2008), are also ichthyo- tioned above, C. subsalsa diverged early from the toxic. Harmful raphidophyte blooms are best documen- lineage with other Chattonella species, whereas C. ted for East Asian waters, where they heavily affect the subsalsa strains from geographically distinct locations extensive fishery and mariculture activities (Toriumi & showed no differences. Takano, 1973; Yoshimatsu, 1987). Nevertheless, raphi- Here we present an analysis to clarify the systema- dophyte blooms have also afflicted other coastal areas tics of C. subsalsa and isolates of Chattonella from the both recently and over the past few decades, including western Adriatic coast. We used five phylogenetic in the Mediterranean Sea (Hollande & Enjumet, 1957; markers: the small subunit (SSU), internal transcribed Tregouboff, 1962; Margalef, 1968; Mikhail, 2007). spacer (ITS) region and large subunit (LSU) of nuclear Tracking raphidophyte distributions in recent rDNA, and
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