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Origin and Evolution of Dinoflagellates with a Diatom Endosymbiont

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Origin and Evolution of Dinoflagellates with a Diatom Endosymbiont Title Origin and Evolution of Dinoflagellates with a Diatom Endosymbiont Author(s) Horiguchi, Takeo Citation Edited by Shunsuke F. Mawatari, Hisatake Okada., 53-59 Issue Date 2004 Doc URL http://hdl.handle.net/2115/38506 Type proceedings International Symposium on "Dawn of a New Natural History - Integration of Geoscience and Biodiversity Studies". 5- Note 6 March 2004. Sapporo, Japan. File Information p53-59-neo-science.pdf Instructions for use Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP Origin and Evolution of Dinoflagellates with a Diatom Endosymbiont Takeo Horiguchi Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo 060-0810, Japan ABSTRACT The origin and evolutionary scenario of a small group of dinoflagellates with unusual chloroplasts are discussed. These dinoflagellates are known to possess an endosymbiotic alga of diatom origin. These are Durinskia baltica, Kryptoperidinium foliaceum, Peridinium quinquecorne, Durinskia sp., Gymnodinium quadrilobatum, Peridiniopsis rhomboids, Dinothrix paradoxa and a new coccoid di- noflagellate from Palau (P-18 strain). Although these eight species share a similar type of endosym- biont, morphologically they are so diverse that they may be classified as different entities, even to the ordinal level, using the current taxonomic criteria. To investigate the origin(s) and phylogenetic affinities of these dinoflagellates, the SSU rRNA and rbcL genes of D. baltica, K foliaceum, Durinskia sp., Peridiniopsis rhomboids, Dinothrix paradoxa and P-18 strain were sequenced and analysed. Phylogenetic trees based on nuclear encoded SSU rRNA gene strongly suggested that all these endosymbiotic dinoflagellates are monophyletic. The phylogenetic analyses based on the plas- tid encoded rbcL gene also revealed that all the endosymbiotic algae formed a unique clade within the diatom clade. Therefore, the acquisition of the endosymbiont took place only once and species diversified later. Of the diatoms included in the alignment, a pennate diatom, Nitzschia longissima var. reversa (Bacillariaceae) was shown to be the closest relative of the dinoflagellate endosymbionts. According to the fossil record, the members of the genus Nitzschia first appeared in Late Oligocene to Early Miocene and therefore, establishment of this endosymbiotic event must have been post this era. The evolutionary scenario of these dinoflagellates after establishment of the endosymbiont has been presented. Keywords: Chloroplast, Diatom, Dinoflagellate, Endosymbiosis, Eyespot types and these different types of chloroplasts are INTRODUCTION thought to have been derived from different endo- The dinoflagellates are a group of protists, com- symbiotic events [1]. prising extremely diverse (morphologically, cytologi- The origin and evolutionary scenario of one such cally and physiologically) assemblages. About half group of dinoflagellates with unusual chloroplasts of the dinoflagellate species are photosynthetic and will be dealt here. It is a relatively small group of di- their chloroplasts are characterized by 1) being tri- noflagellates known to possess an endosymbiotic ple membrane bound and 2) containing peridinin as alga of diatom origin. These include Durinskia a major xanthophyll, in addition to chlorophylls a/c. baltica [2], Kryptoperidinium foliaceum [3], Peridin- There are, however, exceptions to this rule. Some di- ium quinquecorne [4], Durinskia sp.[5], Gymnodin- noflagellates possess chloroplasts of totally different ium quadrilobatum [6], and Dinothrix paradoxa [7]. Mawatari, S. F. & Okada, H. (eds.), Neo-Science of Natural History: Integration of Geoscience and Biodiversity Stud- ies, Proceedings of International Symposium on "Dawn of a New Natural History - Integration of Geoscience and Biodiversity Studies", March 5-6, 2004, Sapporo, pp. 53-59. 54 T. Horiguchi In these organisms, the dinoflagellate cytoplasm and Kryptoperidinium foliaceum (Stein) Lindemann the endosymbiont cytoplasm are separated by a sin- (order Peridiniales) Fig. lc gle unit membrane. The endosymbiont cytoplasm is A highly flattened, motile marine dinoflagellate. rather simple and includes only a nucleus, chloro- This is also a well known species as a diatom-har- plasts and mitochondria [2]. The host-endosymbiont boring dinoflagellate and extensively studied just relationship is a permanent one as it is no longer like D. baltica. The thecal plate arrangement is: Po, possible to separate these two cellular components. x, 4', 2a, 7", 5c, 5s, 5"', 2"". This thecal plate ar- Although these six species share a similar type of en- rangement is quite similar to that of Durinskia. How- dosymbiont, morphologically they are so diverse ever, the number of precingular plates is different (7 that they may be classified as different entities, even vs. 6) [3, 9-11, 13-14, 15]. The strain used in this to the ordinal level, using the present taxonomic study is from culture collection of UTEX. system. To investigate the origin(s) and phyloge- netic affinities of these dinoflagellates, the SSU Peridinium quinquecorne Abe (order Peridinia- rRNA and rbcL genes of D. baltica, K. foliaceum, les) Fig. ld Durinskia sp. and Dinothrix paradoxa were se- A characteristic motile dinoflagellate with promi- quenced and analysed. The same genes in a non- nent antapical spines. The thecal plate arrangement motile, coccoid, dinoflagellate with a similar endo- is: Po, x, 3', 2a, 7", 5c, 4s, 5"', 2"". Unfortunate- symbiont from Palau (P18 strain, a new taxon) and a ly, it has not been possible to sequence this species freshwater, bloom-forming dinoflagellate, Perid- to date. This species has been found from many iniopsis rhomboides were also analysed. places along Japanese coast, including Lake Hamana. RESULTS AND DISCUSSION Peridiniopsis rhomboides Krakhmalny (order Pe- Diversity of Dinoflagellates with a Diatom Endo- ridiniales) Fig. le symbiont This species was found to produce blooms in a The following eight species are now recognized freshwater pond in Toyama Prefecture, central Japan as the dinoflagellates with a diatom endosymbiont. in the spring/summer of the year 2003. The thecal Although it is not the aim of this paper to go into de- plate arrangement is: Po, x, 4', Oa, 6", ?c. ?s, 5"', tails of each species, they are briefly described. 2"". Although we have identified the species as P. rhomboides, its identity needs further study, because Durinskia baltica (Levander) Carty et Cox (order this species is closely related to the species such as Peridiniales) Fig. la Peridiniopsis kevei Grigorszky et al. [ 16] and P. co- Small motile dinoflagellate belonging to the order rillionii Leitao et al. [17] Peridiniales. This is a type species of the genus. The- cal plate arrangement is: Po, x, 4', 2a, 6", 5c, 4s, Gymnodinium quadrilobatum Horiguchi et Pi- 5"', 2"". We found the species both from marine enaar (order Phytodiniales?) Fig. if (Okinawa) and freshwater (Hokkaido) environ- This species has been described from beach sand ments. This is a well known species as a diatom-har- from subtropical Indian Ocean coast of South boring dinoflagellate and extensively studied [2, Africa. This species has also been found from mud 8-12]. of mangrove river in Iriomote Island, Japan. It is characterized by four-leaved-clover like non-motile Durinskia sp. (order Peridiniales) Fig. lb cell. The non-motile cell is dominant in life cycle. It This species has been found from the tide pools reproduces asexually by forming two motile cells. in several localities in South Africa, especially along The motile cell is athecate and Gymnodinium-like in the Cape coast. Thecal plate arrangement is: Po, x, morphology. This is why Horiguchi and Pienaar [5] 4', 2a, 6", 5c, 5s, 5"', 2"". Although the thecal described it as a new species of the genus Gym- plate arrangement is almost same as that of the type nodinium, rather than creating a new genus based on species, gross morphology is very different from the its unique vegetative morphology. However, now latter and therefore, we believe it is a new species. the genus Gymnodinium is strictly defined [ 18] and The formal description of the species is now in the motile cell of this species does not fit the recent preparation. definition of the genus Gymnodinium. Here I tenta- tively treat this species as a member of the order Phytodiniales, which is characterized by having Dinoflagellates with a Diatom Endosymbiont 55 b c d I. 9 MIMPIFIRINIPP— - Fig. 1 Dinoflagellates with a diatom endosymbiont. a. Durinskia baltica, b. Durinskia sp. c. Kryptoperidinium foliaceum, d. Pe- ridinium quinquecorne, e. Peridiniopsis rhomboids, f. Gymnodinium quadrilobatum, g. P-18 strain from Palau, h. Dinothrix paradoxa. Scale bars = 10 ,um dominant non-motile vegetative stage. Unfortunate- cells. The motile cell is athecate. The motile cell di- ly, we have not been able to sequence this species to rectly returns to the non-motile vegetative form. date. This species is probably a new genus and a species (manuscript in preparation). P-18 strain (order Phytodiniales) Fig. lg This newly isolated strain from the bottom sand Dinothrix paradoxa Pascher (order Dinotrichales, of the Jellyfish Lake, Palau, possesses very unique or family Dinocloniaceae, order Phytodiniales) vegetative form. It is helmet-shaped and firmly at- Fig. lh taches to the substratum. The dominant stage in life This dinoflagellate is characteristic because it has cycle is this non-motile, attached form. It repro- pseudo-filamentous form, which consists
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