Discovery of a kleptoplastic 'dinotom' dinoflagellate and the unique nuclear dynamics of converting kleptoplastids to permanent plastids

A monophyletic group of dinoflagellates, called ‘dinotoms’, are known to possess evolutionarily intermediate plastids derived from diatoms. The diatoms maintain their nuclei, mitochondria, and the endoplasmic reticulum in addition with their plastids, while it has been observed that the host dinoflagellates retain the diatoms permanently by controlling diatom karyokinesis. Previously, we showed that dinotoms have repeatedly replaced their diatoms. Here, we show the process of replacements is at two different evolutionary stages in two closely related dinotoms, Durinskia capensis and D. kwazulunatalensis. We clarify that D. capensis is a kleptoplastic protist keeping its diatoms temporarily, only for two months. On the other hand, D. kwazulunatalensis is able to keep several diatoms permanently and exhibits unique dynamics to maintain the diatom nuclei: the nuclei change their morphologies into a complex string-shape alongside the plastids during interphase and these string-shaped nuclei then condense into multiple round nuclei when the host divides. These dynamics have been observed in other dinotoms that possess permanent diatoms, while they have never been observed in any other eukaryotes. We suggest that the establishment of this unique mechanism might be a critical step for dinotoms to be able to convert kleptoplastids into permanent plastids.info:eu-repo/semantics/publishedVersio

Origin and Evolution of Dinoflagellates with a Diatom Endosymbiont

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 dinoflagellate from Palau (P-18 strain). Although these eight species share a similar type of endosymbiont, 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 plastid 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.International Symposium on "Dawn of a New Natural History - Integration of Geoscience and Biodiversity Studies". 5-6 March 2004. Sapporo, Japan

Soil Protists and Soil Animals on Daikokujima

The soil protist and animal fauna of Daikoku-jima Island, North Japan, were surveyed. Testate amoebae, ciliates and flagellates (Protist) were isolated and sequenced for identification. Oribatid mites, collembolans and earthworms were identified under light microscopy. Thirty-five families and 57 species of oribatid mites were recorded. One species and one subspecies were described. Three species were newly recorded from Japan. Seven families and 45 species of collembola were collected from 12 stations. Two families and two species of earthworm were collected and one species of them was redescribed.International Symposium, "The Origin and Evolution of Natural Diversity". 1–5 October 2007. Sapporo, Japan

Morphological Transition in Kleptochloroplasts after Ingestion in the Dinoflagellates Amphidinium poecilochroum and Gymnodinium aeruginosum (Dinophyceae)

The unarmoured marine dinoflagellate Amphidinium poecilochroum and the unarmoured freshwater dinoflagellate Gymnodinium aeruginosum both belonging to the same clade, are known to possess cryptomonad-derived kleptochloroplasts. Previous studies revealed that G. aeruginosum can synchronise the division of the chloroplast with its own cell division while no simultaneous division takes place in A. poecilochroum, which is interpreted to mean that state of kleptochloroplastidy in G. aeruginosum is closer to that of the initial acquisition of the 'true chloroplast' within the lineage. Although the general ultrastructure of these two species has been reported, the changes in the kleptochloroplast with time have never been followed. We observed morphological changes in kleptochloroplasts of A. poecilochroum and G. aeruginosum following the ingestion of cryptomonad cells, using light and transmission electron microscopes. In A. poecilochroum, the cryptomonad ejectosomes, mitochondria and cytoplasm were all actively transferred into digestive vacuoles within 1 h of ingestion. The chloroplasts were deformed and the cryptomonad nucleus was digested after 3 h. By contrast, in G. aeruginosum, the cryptomonad cytoplasm and nucleus were retained for 24 h following ingestion, and the chloroplast was substantially enlarged. These differences imply that the retention of the cryptomonad nucleus is important for the maintenance of the chloroplast. (c) 2013 Elsevier GmbH. All rights reserved

Kleptochloroplast Enlargement, Karyoklepty and the Distribution of the Cryptomonad Nucleus in Nusuttodinium (= Gymnodinium) aeruginosum (Dinophyceae)

The unarmoured freshwater dinoflagellate Nusuttodinium (= Gymnodinium) aeruginosum retains a cryptomonad-derived kleptochloroplast and nucleus, the former of which fills the bulk of its cell volume. The paucity of studies following morphological changes to the kleptochloroplast with time make it unclear how the kleptochloroplast enlarges and why the cell ultimately loses the cryptomonad nucleus. We observed, both at the light and electron microscope level, morphological changes to the kleptochloroplast incurred by the enlargement process under culture conditions. The distribution of the cryptomonad nucleus after host cell division was also investigated. The volume of the kleptochloroplast increased more than 20-fold, within 120 h of ingestion of the cryptomonad. Host cell division was not preceded by cryptomonad karyokinesis so that only one of the daughter cells inherited a cryptomonad nucleus. The fate of all daughter cells originating from a single cell through five generations was closely monitored, and this observation revealed that the cell that inherited the cryptomonad nucleus consistently possessed the largest kleptochloroplast for that generation. Therefore, this study suggests that some important cryptomonad nucleus division mechanism is lost during ingestion process, and that the cryptomonad nucleus carries important information for the enlargement of the kleptochloroplast

Specificity of Chroomonas (Cryptophyceae) as a source of kleptochloroplast for Nusuttodinium aeruginosum (Dinophyceae)

The unarmoured dinoflagellate Nusuttodinium aeruginosum retains a kleptochloroplast, which is a transient chloroplast stolen from members of the cryptomonad genus, Chroomonas. Both N.aeruginosum and the closely related N.acidotum have been shown to restrict their diet to a limited number of species of this blue-green genus of cryptophyte. However, it is still unclear how flexible the predators are with regard to the ingestion and utilization of Chroomonas spp. as a source of kleptochloroplast. To address specificity of cryptomonad in N.aeruginosum, we collected the cells of N.aeruginosum from several ponds in Japan, and analysed the phylogeny of the kleptochloroplasts based on their plastidial 16S rDNA sequences. All sequences obtained in this study were restricted to only one (the subclade 4) of four subclades known to comprise the Chroomonas/Hemiselmis clade. Therefore, N.aeruginosum is specific in its dietary requirements, selecting their prey within the subclade level

Species of the Parasitic Genus Duboscquella are Members of the Enigmatic Marine Alveolate Group I

Small subunit ribosomal RNA gene sequences of Duboscquella spp. infecting the tintinnid ciliate, Favella ehrenbergii, were determined. Two parasites were sampled from different localities. They are morphologically similar to each other and both resemble D. aspida. Nevertheless, two distinct sequences (7.6% divergence) were obtained from them. Phylogenetic trees inferred from maximum likelihood and maximum parsimony revealed that these two Duboscquella spp. sequences are enclosed in an environmental clade named Marine Alveolate Group I. This clade consists of a large number of picoplanktonic organisms known only from environmental samples from various parts of the ocean worldwide, and which therefore lack clear characterization and identification. Here, we provide morphological and genetic characterization of these two Duboscquella genotypes included in this enigmatic clade. Duboscquella spp. produce a large number of small flagellated spores as dispersal agents and the presence of such small cells partially explains why the organisms related to these parasites have been detected within environmental genetic libraries, built from picoplanktonic size fractions of environmental samples. The huge diversity of the Marine Alveolate Group I and the finding that parasites from different marine protists belong to this lineage suggest that parasitism is a widespread and ecologically relevant phenomenon in the marine environment

Pigment compositions are linked to the habitat types in dinoflagellates

Compared to planktonic species, there is little known about the ecology, physiology, and existence of benthic dinoflagellates living in sandy beach or seafloor environments. In a previous study, we discovered 13(2),17(3)-cyclopheophorbide a enol (cPPB-aE) from sand-dwelling benthic dinoflagellates. This enol had never been detected in phytoplankton despite the fact that it is a chlorophyll a catabolite. We speculated from this discovery that habitat selection might be linked to pigment compositions in dinoflagellates. To test the hypothesis of habitat selection linking to pigment compositions, we conducted extensive analysis of pigments with high performance liquid chromatography (HPLC) for 40 species using 45 strains of dinoflagellates including three habitat types; sand-dwelling benthic forms, tidal pool inhabitants and planktonic species. The 40 dinoflagellates are also able to be distinguished into two types based on their chloroplast origins; red alga-derived secondary chloroplasts and diatom-derived tertiary ones. By plotting the pigments profiles onto three habitats, we noticed that twelve pigments including cPPB-aE were found to occur only in benthic sand-dwelling species of red alga-derived type. The similar tendency was also observed in dinoflagellates with diatom-derived chloroplasts, i.e. additional sixteen pigments including chl c (3) were found only in sand-dwelling forms. This is the first report of the occurrence of chl c (3) in dinoflagellates with diatom-derived chloroplasts. These results clarify that far greater diversity of pigments are produced by the dinoflagellates living in sand regardless of chloroplast types relative to those of planktonic and tidal pool forms. Dinoflagellates seem to produce a part of their pigments in response to their habitats

Pseudo-cryptic speciation in Braarudosphaera bigelowii (Gran and Braarud) Deflandre

Partial SSU rDNA sequences were obtained from 13 naturally collected cells of Braarudosphaera bigelowii obtained from various parts of seas surrounding Japan. Together with the two previously reported sequences, 15 specimens were classified into five SSU rDNA Genotypes I-V. Based on the side length of the pentaliths forming the coccosphere, these specimens were also classified into three size-morphotypes; Intermediate form-A, Intermediate form-B, and Large form. Genotypes of B. bigelowii were well correlated with size-morphotypes but not with sampling area. This result indicates that size differences in B. bigelowii are the results of speciation and not of intra-population variety. Therefore, Genotypes I and II (Intermediate form-A) and Genotypes IV and V (Large form) are regarded as pseudo-cryptic sibling species of typical B. bigelowii (Genotype III, Intermediate form-B), which corresponds to the original description of the species. From the SSU rDNA sequences, it is evident that Genotype V arose from Genotype IV, and Genotype IV originated from Genotype III. The specimens of Genotypes III-V showed size increase of pentaliths in accordance with their branching order. The consistency in the relationship between genotypes and size-morphotypes of living B. bigelowii-complex observed in this study suggests that inconsistency of size range of 'B. bigelowii' pentaliths among different geological ages reported by palaeontological studies stems from additional pseudo-cryptic speciation in the lineage of 'B. bigelowii' in the geological past