A Novel Type of Kleptoplastidy in (Dinophyceae): Presence of Haptophyte-type Plastid in

Koike, Kazuo; Sekiguchi, Hiroshi; Kobiyama, Atsushi; Takishita, Kiyotaka; Kawachi, Masanobu; Koike, Kanae; Ogata, Toru

doi:10.1016/j.protis.2005.04.002

Cited by 65 publications

(54 citation statements)

References 39 publications

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“…The genus Dinophysis has a number of species known to harbor plastids of cryptophycean origin (Hallegraeff and Lucas 1988), and at least one species, D. mitra, which possesses haptophyte algal plastids (Koike et al 2005). Field populations of Dinophysis spp.…”

Section: Organelle-retaining Dinoflagellatesmentioning

confidence: 99%

The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

2010

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Many non-photosynthetic species of protists and metazoans are capable of hosting viable algal endosymbionts or their organelles through adaptations of phagocytic pathways. A form of mixotrophy, acquired phototrophy (AcPh) encompasses a sweet of endosymbiotic and organelle retention interactions, that range from facultative to obligate. AcPh is a common phenomenon in aquatic ecosystems, with endosymbiotic associations generally more prevalent in nutrient poor environments, and organelle retention typically associated with more productive ones. All AcPhs benefit from enhanced growth due to access to photosynthetic products, however the degree of metabolic integration and dependency in the host varies widely. AcPhs are mixotrophic, using both heterotrophic and phototrophic carbon sources. AcPh is found in at least four of the major eukaryotic supergroups, and is the driving force in the evolution of secondary and tertiary plastid acquisitions. Mutualistic resource partitioning characterizes most algal endosymbiotic interactions, while organelle retention is a form of predation, characterized by nutrient flow (i.e. growth) in one direction. AcPh involves adaptations to recognize specific prey or endosymbionts and to house organelles or endosymbionts within the endomembrane system but free from digestion. In many cases, hosts depend upon AcPh for the production of essential nutrients, many of which remain obscure. The practice of AcPh has led to multiple independent secondary and tertiary plastid acquisition events among several eukaryote lineages, giving rise to the diverse array of algae found in modern aquatic ecosystems.This review highlights those AcPhs that are model research organisms for both metazoans and protists.Much of the basic biology of AcPhs remains enigmatic, particularly 1) which essential nutrients or factors make certain forms of AcPh obligatory, 2) how hosts regulate and manipulate endosymbionts or sequestered organelles, and 3) what genomic imprint, if any, AcPh leaves on non-photosynthetic host species.2

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Section: Organelle-retaining Dinoflagellatesmentioning

confidence: 99%

The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

2010

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“…An endosymbiosis is considered to be stable if there is genetic integration of the endosymbiont and host, meaning transfer of essential endosymbiont genes to the host nucleus and protein retargeting (Bhattacharya et al 2007). For example, Dinophysis has long been considered to have a cryptophyte endosymbiont chloroplast, but the latter was very recently found to have been acquired through kleptoplastidy (Koike et al 2005;Minnhagen and Janson 2006;Takishita et al 2002).…”

Section: Introductionmentioning

confidence: 99%

The Life History and Cell Cycle of Kryptoperidinium foliaceum, A Dinoflagellate with Two Eukaryotic Nuclei

Figueroa

Bravo

Fraga

et al. 2009

Protist

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Kryptoperidinium foliaceum is a binucleate dinoflagellate that contains an endosymbiont nucleus of diatom origin. However, it is unknown whether the binucleate condition is permanent or not and how the diatom nucleus behaves during the life history processes. In this sense, it is also unknown if there is a sexual cycle or a resting stage during the life history of this species, two key aspects necessary to understand the life history strategy of this dinoflagellate. To answer these questions, life history and cell cycle studies were performed with the following results: (i) Kryptoperidinium foliaceum has a sexual cycle and in the dinoflagellate strains studied, the binucleate condition is permanent. Sexuality in the host was confirmed by the presence of fusing gamete pairs and planozygotes in clonal cultures (revealing homothallism), but signs of meiosis in the endosymbiont were not observed. The endosymbiont nucleus likely fuses first, because fusing gamete pairs were found to have two dinoflagellate nuclei but only one endosymbiont nucleus. After complete gamete fusion, the planozygotes had apparently normal endosymbiont and dinoflagellate nuclei. (ii) Asexual division studies using flow cytometry showed that the S phase in the endosymbiont (diatom) nucleus starts 6-8 h later than in the host nucleus, but there was no evidence of mitosis in the former. (iii) Sexual and asexual cysts were formed in culture. Neither cysts from natural samples nor those formed in culture exhibited a dormancy period before germination.

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“…In recent years, it has become clear that plastid sequences of the 16S rRNA gene and psbA (encoding the photosystem II [PSII] reaction center protein D1) in natural Dinophysis cells (except Dinophysis mitra) (27) originate from the cryptophyte genus complex Teleaulax/Geminigera/Plagioselmis (19,35,49,50). Minnhagen and Janson (35) have also reported an exception to this finding in that natural D. acuminata cells isolated from the Greenland Sea contained a plastid 16S rRNA gene sequence that was more closely related to Geminigera cryophila.…”

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confidence: 99%

High-Level Congruence of Myrionecta rubra Prey and Dinophysis Species Plastid Identities as Revealed by Genetic Analyses of Isolates from Japanese Coastal Waters

Nishitani

Nagai

Baba

et al. 2010

Appl Environ Microbiol

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We analyzed cryptophyte nucleomorph 18S rRNA gene sequences retained in natural Myrionecta rubra cells and plastid 16S rRNA gene and psbA sequences retained in natural cells of several Dinophysis species collected from Japanese coastal waters. A total of 715 nucleomorph sequences obtained from 134 M. rubra cells and 564 plastid 16S rRNA gene and 355 psbA sequences from 71 Dinophysis cells were determined. Almost all sequences in M. rubra and Dinophysis spp. were identical to those of Teleaulax amphioxeia, suggesting that M. rubra in Japanese coastal waters preferentially ingest T. amphioxeia. The remaining sequences were closely related to those of Geminigera cryophila and Teleaulax acuta. Interestingly, 37 plastid 16S rRNA gene sequences, which were different from T. amphioxeia and amplified from Dinophysis acuminata and Dinophysis norvegica cells, were identical to the sequence of a D. acuminata cell found in the Greenland Sea, suggesting that a widely distributed and unknown cryptophyte species is also preyed upon by M. rubra and subsequently sequestered by Dinophysis. To confirm the reliability of molecular identification of the cryptophyte Teleaulax species detected from M. rubra and Dinophysis cells, the nucleomorph and plastid genes of Teleaulax species isolated from seawaters were also analyzed. Of 19 isolates, 16 and 3 clonal strains were identified as T. amphioxeia and T. acuta, respectively, and no sequence variation was confirmed within species. T. amphioxeia is probably the primary source of prey for M. rubra in Japanese coastal waters. An unknown cryptophyte may serve as an additional source, depending on localities and seasons.The marine dinoflagellate genus Dinophysis comprises photosynthetic and nonphotosynthetic members and is globally distributed in coastal and oceanic waters (12,29,30). Several members of the genus Dinophysis produce potent polyether toxins that can accumulate in filter-feeding bivalves, leading to a syndrome known as diarrhetic shellfish poisoning (DSP) in humans who consume tainted shellfish. These toxic algal species are important not only for their potential impact on public health but also from an ecological point of view because of their dual role as primary and secondary producers in complex microbial food webs. Despite extensive studies over the last 2 decades, little is known about the ecophysiology, toxicology, and bloom mechanisms of DSP-causing species of Dinophysis, primarily due to an inability to culture them. Since the first successful cultivation of Dinophysis acuminata by Park et al. (42), the understanding of Dinophysis biology and ecology has progressed considerably. Three other species (Dinophysis caudata, Dinophysis fortii, and Dinophysis infundibulus) are now available in culture, and it has become clear that these different Dinophysis species require the presence of both cryptophytes and the marine ciliate Myrionecta rubra to grow and proliferate (36,37,38). When presented with the marine ciliate M. rubra as prey, the four Dinophysis species mentioned...

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A Novel Type of Kleptoplastidy in (Dinophyceae): Presence of Haptophyte-type Plastid in

Cited by 65 publications

References 39 publications

The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles

The Life History and Cell Cycle of Kryptoperidinium foliaceum, A Dinoflagellate with Two Eukaryotic Nuclei

High-Level Congruence of Myrionecta rubra Prey and Dinophysis Species Plastid Identities as Revealed by Genetic Analyses of Isolates from Japanese Coastal Waters

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