The extraordinary longevity of kleptoplasts derived from the Ross Sea haptophyte Phaeocystis antarctica within dinoflagellate host cells relates to the diminished role of the oxygen-evolving Photosystem II and to supplementary light harvesting by mycosporine-like amino acid/s

Stamatakis, Kostas; Vayenos, Dimitris; Kotakis, Christos; Gast, Rebecca J.; Papageorgiou, George C.

doi:10.1016/j.bbabio.2016.12.002

Cited by 9 publications

(7 citation statements)

References 36 publications

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“…In contrast, however, we did not find a single subunit of photosystem II (PSII) in the RSD nucleus, whereas P. antarctica encodes several (SI Appendix, Table S2). This correlates with measurements showing a severely diminished PSII activity in the kleptoplast compared to P. antarctica plastids (44).…”

Section: Resultssupporting

confidence: 87%

A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis

Hehenberger

Gast

Keeling

2019

Proc. Natl. Acad. Sci. U.S.A.

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Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because dinoflagellate plastids have repeatedly been reduced, lost, and replaced by new plastids, leading to a spectrum of ages and integration levels. Here we describe deep-transcriptomic analyses of the Antarctic Ross Sea dinoflagellate (RSD), which harbors long-term but temporary kleptoplasts stolen from haptophyte prey, and is closely related to dinoflagellates with fully integrated plastids derived from different haptophytes. In some members of this lineage, called the Kareniaceae, their tertiary haptophyte plastids have crossed a tipping point to stable integration, but RSD has not, and may therefore reveal the order of events leading up to endosymbiotic integration. We show that RSD has retained its ancestral secondary plastid and has partitioned functions between this plastid and the kleptoplast. It has also obtained genes for kleptoplast-targeted proteins via horizontal gene transfer (HGT) that are not derived from the kleptoplast lineage. Importantly, many of these HGTs are also found in the related species with fully integrated plastids, which provides direct evidence that genetic integration preceded organelle fixation. Finally, we find that expression of kleptoplast-targeted genes is unaffected by environmental parameters, unlike prey-encoded homologs, suggesting that kleptoplast-targeted HGTs have adapted to posttranscriptional regulation mechanisms of the host.

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Section: Resultssupporting

confidence: 87%

A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis

Hehenberger

Gast

Keeling

2019

Proc. Natl. Acad. Sci. U.S.A.

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“…Specifically, the MAAs within the plastids may act as light-harvesting supplements in the photosynthetic organisms through the F€ orster resonance energy transfer (FRET) mechanism. As the efficiency of FRET depends strongly on the fluorescence yield of the donor and on the proximity to the acceptor, our observations are in line with the hypothetically significant contributions to the energy transfer within the organelle rather than in the more fluidic cytoplasm environment, even considering similar distances between the MAAs and chlorophylls (27).…”

Section: Resultssupporting

confidence: 84%

“…This work aims to evaluate comparatively the UV photoprotective ability and photophysical properties of one form of derivatized shinorine shown in Fig. 1, the shinorine dimethyl ester (SDME), in aqueous solution and in the presence of direct *Corresponding author email: schurio@mdp.edu.ar (M. S. Churio) †This article is part of a Special Issue commemorating the XIII ELAFOT Conference (23)(24)(25)(26)(27) October 2017 -Villa Carlos Paz, Cordoba, Argentina). © 2018 The American Society of Photobiology micelles prepared with CTAC and with sodium dodecyl sulfate (SDS), that is, a cationic and an anionic detergent, respectively.…”

Section: Introductionmentioning

confidence: 99%

Photochemistry and Photophysics of Shinorine Dimethyl Ester

Orallo

Fangio

Poblet

et al. 2018

Photochem & Photobiology

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The photostability and photophysical properties of the dimethyl ester of the mycosporine-like amino acid shinorine have been experimentally evaluated in aqueous solution and in the presence of direct micelles prepared with a cationic or an anionic detergent, respectively. In comparison with shinorine, the ester molecule increases the photostability, the fluorescence quantum yield and the fluorescence lifetime in water as well as in the micellar solutions. The effects are more pronounced in sodium dodecyl sulfate solutions and suggest that the electrostatic attractions with the micellar interface contribute to limit the movement of the molecules and influence the relative rate of their deactivation channels. However, the predominance of the nonradiative decay is maintained together with the UV photoprotective ability of this atypical mycosporine species.

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“…These results suggest that the dinoflagellate cell is unable to maximize the potential of the cryptomonad chloroplast. In a similar manner, in another dinoflagellate species that possesses a kleptoplast derived from a haptophyte, the photosynthetic activity of the haptophyte was reduced after it was ingested by the dinoflagellate [ 63 ].…”

Section: Discussionmentioning

confidence: 99%

Changes in the transcriptome, ploidy, and optimal light intensity of a cryptomonad upon integration into a kleptoplastic dinoflagellate

et al. 2020

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Endosymbiosis of unicellular eukaryotic algae into previously nonphotosynthetic eukaryotes has established chloroplasts in several eukaryotic lineages. In addition, certain unicellular organisms in several different lineages ingest algae and utilize them as temporal chloroplasts (kleptoplasts) for weeks to months before digesting them. Among these organisms, the dinoflagellate Nusuttodinium aeruginosum ingests the cryptomonad Chroomonas sp. and enlarges the kleptoplast with the aid of the cryptomonad nucleus. To understand how the cryptomonad nucleus is remodeled in the dinoflagellate, here we examined changes in the transcriptome and ploidy of the ingested nucleus. We show that, after ingestion, genes involved in metabolism, translation, and DNA replication are upregulated while those involved in sensory systems and cell motility are downregulated. In the dinoflagellate cell, the cryptomonad nucleus undergoes polyploidization that correlates with an increase in the mRNA levels of upregulated genes. In addition, the ingested nucleus almost loses transcriptional responses to light. Because polyploidization and loss of transcriptional regulation are also known to have occurred during the establishment of endosymbiotic organelles, these changes are probably a common trend in endosymbiotic evolution. Furthermore, we show that the kleptoplast and dinoflagellate are more susceptible to high light than the free-living cryptomonad but that the ingested nucleus reduces this damage.

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The extraordinary longevity of kleptoplasts derived from the Ross Sea haptophyte Phaeocystis antarctica within dinoflagellate host cells relates to the diminished role of the oxygen-evolving Photosystem II and to supplementary light harvesting by mycosporine-like amino acid/s

Abstract: The haptophyte Phaeocystis antarctica and the novel Ross Sea dinoflagellate that hosts kleptoplasts derived from P. antarctica (RSD; R.J. Gast et al., 2006, J. Phycol. 42 233-242) were compared for photosynthetic light harvesting and for oxygen evolution activity. Both

Cited by 9 publications

References 36 publications

A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis

A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis

Photochemistry and Photophysics of Shinorine Dimethyl Ester

Changes in the transcriptome, ploidy, and optimal light intensity of a cryptomonad upon integration into a kleptoplastic dinoflagellate

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