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Secondary plastids derived from green algae occur in chlorarachniophytes, photosynthetic euglenophytes, and the dinoflagellate genus Lepidodinium . Recent advances in understanding the origin of these plastids have been made, but analyses suffer from relatively sparse taxon sampling within the green algal groups to which they are related. In this study we aim to derive new insights into the identity of the plastid donors, and when in geological time the independent endosymbiosis events occurred. We use newly sequenced green algal chloroplast genomes from carefully chosen lineages potentially related to chlorarachniophyte and Lepidodinium plastids, combined with recently published chloroplast genomes, to present taxon-rich phylogenetic analyses to further pinpoint plastid origins. We integrate phylogenies with fossil information and relaxed molecular clock analyses. Our results indicate that the chlorarachniophyte plastid may originate from a precusor of siphonous green algae or a closely related lineage, whereas the Lepidodinium plastid originated from a pedinophyte. The euglenophyte plastid putatively originated from a lineage of prasinophytes within the order Pyramimonadales. Our molecular clock analyses narrow in on the likely timing of the secondary endosymbiosis events, suggesting that the event leading to Lepidodinium likely occurred more recently than those leading to the chlorarachniophyte and photosynthetic euglenophyte lineages.

The bloom-forming dinoflagellates and euglenophyceae were observed in the coastal waters of Hammam-Lif (Southern Mediterranean), during a green tide event on 3 June 2023. The bloom was dominated by Lepidodinium chlorophorum, identified through ribotyping with densities reaching 2.3 × 107 cells·L−1. Euglena spp. and Eutrepsiella spp. contributed to the discoloration, with abundances up to 2.9 × 107 cells·L−1. Environmental data revealed significant depletion of nitrite and nitrate, coinciding with a rapid increase in sunlight duration, likely promoting the proliferation of L. chlorophorum and euglenophyceae. By 5 June, two days after the bloom, nutrient stocks were exhausted. Diatoms appeared limited by low silicate concentrations (<0.05 µmol·L−1), while dissolved inorganic phosphate and Nitrogen-ammonia were elevated during the bloom (0.88 and 4.8 µmol·L−1, respectively), then decreased significantly afterward (0.23 and 1.06 µmol·L−1, respectively). Low salinity (34.0) indicated substantial freshwater input from the Meliane River, likely contributing to nutrient enrichment and bloom initiation. After the event, phytoplankton abundance and chlorophyll levels declined, with a shift from dinoflagellates to diatoms. The accumulation of pigments (chlorophyll b and carotenoids) and the presence of Mycosporine-like amino acids (MAAs) during and after the bloom suggest that UV radiation and Nitrogen-ammonia were key drivers of this green tide.

Abstract Endosymbiosis, the establishment of a former free-living prokaryotic or eukaryotic cell as an organelle inside a host cell, can dramatically alter the genomic architecture of the endosymbiont. Plastids or chloroplasts, the light-harvesting organelle of photosynthetic eukaryotes, are excellent models to study this phenomenon because plastid origin has occurred multiple times in evolution. Here, we investigate the genomic signature of molecular processes acting through secondary plastid endosymbiosis—the origination of a new plastid from a free-living eukaryotic alga. We used phylogenetic comparative methods to study gene loss and changes in selective regimes on plastid genomes, focusing on green algae that have given rise to three independent lineages with secondary plastids (euglenophytes, chlorarachniophytes, and Lepidodinium). Our results show an overall increase in gene loss associated with secondary endosymbiosis, but this loss is tightly constrained by the retention of genes essential for plastid function. The data show that secondary plastids have experienced temporary relaxation of purifying selection during secondary endosymbiosis. However, this process is tightly constrained, with selection relaxed only relative to the background in primary plastids. Purifying selection remains strong in absolute terms even during the endosymbiosis events. Selection intensity rebounds to pre-endosymbiosis levels following endosymbiosis events, demonstrating the changes in selection efficiency during different origin phases of secondary plastids. Independent endosymbiosis events in the euglenophytes, chlorarachniophytes, and Lepidodinium differ in their degree of relaxation of selection, highlighting the different evolutionary contexts of these events. This study reveals the selection–drift interplay during secondary endosymbiosis and evolutionary parallels during organellogenesis.

Mixotrophs are widely distributed in aquatic ecosystems and play critical roles in the planktonic food web. However, how mixotrophs respond to projected ocean warming remains a debatable topic. To close the knowledge gap, we investigated the thermal responses of growth rate and functional traits of a mixotrophic dinoflagellate (Lepidodinium sp.) isolated from subtropical coastal waters. We found that Lepidodinium sp. is a facultative mixotroph with an obligate phototrophic lifestyle that adjusts its phagocytotic feeding according to inorganic nutrient concentrations. The thermal sensitivity in terms of activation energy (Eₐ, eV) of Lepidodinium sp. grown in mixotrophic mode (with sufficient prey, 0.69–0.89 eV) was significantly higher than in autotrophic mode (without prey, 0.30–0.37 eV). This finding is consistent with the results of predominantly heterotrophic mixotrophs, providing experimental evidence for the hypothesis that mixotrophs shift towards more heterotrophy with rising temperatures. Warming stimulated a higher growth rate of Lepidodinium sp. grown in mixotrophic conditions than in autotrophic conditions, indicating that mixotrophic dinoflagellates may benefit substantially from mixotrophy when temperature increases and prey is sufficient. Moreover, the cell size of both autotrophic and mixotrophic Lepidodinium sp. decreased with increasing temperature. The N:P and C:P ratios of Lepidodinium sp. did not vary with temperature, while the C:N ratio slightly increased. Our results suggest that mixotrophs like Lepidodinium sp. would become more heterotrophic with higher growth rates in warming oceans. The subsequent changes in their functional role from primary producers to consumers may affect food web dynamics and carbon and nutrient cycling.

Dinoflagellates possess plastids that are diverse in both pigmentation and evolutionary background. One of the plastid types found in dinoflagellates is pigmented with chlorophylls a and b (Chl a + b ) and originated from the endosymbionts belonging to a small group of green algae, Pedinophyceae. The Chl a + b -containing plastids have been found in three distantly related dinoflagellates Lepidodinium spp., strain MGD, and strain TGD, and were proposed to be derived from separate partnerships between a dinoflagellate (host) and a pedinophycean green alga (endosymbiont). Prior to this study, a plastid genome sequence was only available for L. chlorophorum , which was reported to bear the features that were not found in that of the pedinophycean green alga Pedinomonas minor , a putative close relative of the endosymbiont that gave rise to the current Chl a + b -containing plastid. In this study, we sequenced the plastid genomes of strains MGD and TGD to compare with those of L. chlorophorum as well as pedinophycean green algae. The mapping of the RNA-seq reads on the corresponding plastid genome identified RNA editing on plastid gene transcripts in the three dinoflagellates. Further, the comparative plastid genomics revealed that the plastid genomes of the three dinoflagellates achieved several features, which are not found in or much less obvious than the pedinophycean plastid genomes determined to date, in parallel.

High biomasses of the marine dinoflagellate Lepidodinium chlorophorum cause green seawater discolorations along Southern Brittany (NE Atlantic, France). The viscosity associated to these phenomena has been related to problems in oyster cultivation. The harmful effect of L. chlorophorum might originate from the secretion of Extracellular Polymeric Substances (EPS). To understand whether the EPS are produced by L. chlorophorum or its associated bacteria, or if they are a product of their interaction, batch cultures were performed under non-axenic and pseudo-axenic conditions for three strains. Maximum dinoflagellate cell abundances were observed in pseudo-axenic cultures. The non-sinking fraction of polymers (Soluble Extracellular Polymers, SEP), mainly composed of proteins and the exopolysaccharide sulphated galactan, slightly increased in pseudo-axenic cultures. The amount of Transparent Exopolymer Particles (TEP) per cell increased under non-axenic conditions. Despite the high concentrations of Particulate Organic Carbon (POC) measured, viscosity did not vary. These results suggest that the L. chlorophorum -bacteria interaction could have a detrimental consequence on the dinoflagellate, translating in a negative effect on L. chlorophorum growth, as well as EPS overproduction by the dinoflagellate, at concentrations that should not affect seawater viscosity.

R. Siano, W.H.C.F. Kooistra, M. Montresor and A. Zingone. 2009. Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia 48: 44-65. DOI: 10.2216/08-61.1. The unarmoured dinoflagellate assemblage of the Gulf of Naples has been investigated in the frame of a 1-year sampling of natural surface samples collected weekly at a coastal station c. 2 miles offshore. Twenty-six strains of unarmoured dinoflagellates were brought into culture by means of serial dilution. Observations at both light and scanning electron microscopy (SEM) together with molecular phylogenetic analyses allowed identification of eight dinoflagellate species. Gymodinium aureolum, Karlodinium veneficum, Protodinium simplex and Takayama acrotrocha were previously reported in the Mediterranean; whereas, Karlodinium ballantinum and Lepidodinium viride together with a taxon identified as Karenia cf. longicanalis are recorded in the basin for the first time. A new thin-walled dinoflagellate is described as Woloszynskia cincta sp. nov. on the basis of morphological results. Molecular analysis showed that Woloszynskia cincta is closely related to W. halophila and W. pseudopalustris and only distantly related to W. pascheri. In Protodinium simplex, a straight acrobase and an arrangement of the amphiesmal vesicles in latitudinal series were revealed by SEM observations, demonstrating the relatedness of this species with woloszynskioid dinoflagellates. Based on new morphological information on Karlodinium species, Gyrodinium corsicum is transferred to Karlodinium corsicum. New morphological features are identified for the recognition of Takayama acrotrocha, such as the arrangement of the acrobase and the presence of a pore on the ventral side of the cell. The latter species was found to be genetically distinct from other species in the genus Takayama, which is monophyletic.

The shift between photoautotrophic and phagotrophic strategies in mixoplankton significantly impacts the planktonic food webs and biogeochemical cycling. Considering the projected global warming, studying how temperature impacts this shift is crucial. Here, we combined the transcriptome of in-lab cultures (mixotrophic dinoflagellate Lepidodinium sp.) and the metatranscriptome dataset of the global ocean to investigate the mechanisms underlying the shift of trophic strategies and its relationship with increasing temperatures. Our results showed that phagocytosis-related pathways, including focal adhesion, regulation of actin cytoskeleton, and oxidative phosphorylation, were significantly stimulated in Lepidodinium sp. when cryptophyte prey were added. We further compared the expression profiles of photosynthesis and phagocytosis genes in Lepidodinium sp. in the global sunlit ocean. Our results indicated that Lepidodinium sp. became more phagotrophic with increasing temperatures when the ambient chlorophyll concentration was >0.3 mg.m−3 (~20.58% of the ocean surface) but became more photoautotrophic with increasing temperatures when the chlorophyll concentration was between 0.2 and 0.3 mg.m−3 (~11.47% of the ocean surface). Overall, we emphasized the crucial role of phagocytosis in phago-mixotrophy and suggested that the expression profile of phagocytosis genes can be a molecular marker to target the phagotrophic activity of mixoplankton in situ.

Background\\nThe ancestral dinoflagellate most likely established a peridinin-containing plastid, which have been inherited in the extant photosynthetic descendants. However, kareniacean dinoflagellates and Lepidodinium species were known to bear \"non-canonical\" plastids lacking peridinin, which were established through haptophyte and green algal endosymbioses, respectively. For plastid function and maintenance, the aforementioned dinoflagellates were known to use nucleus-encoded proteins vertically inherited from the ancestral dinoflagellates (vertically inherited- or VI-type), and those acquired from non-dinoflagellate organisms (including the endosymbiont). These observations indicated that the proteomes of the non-canonical plastids derived from a haptophyte and a green alga were modified by \"exogenous\" genes acquired from non-dinoflagellate organisms. However, there was no systematic evaluation addressing how \"exogenous\" genes reshaped individual metabolic pathways localized in a non-canonical plastid.\\nResults\\nIn this study, we surveyed transcriptomic data from two kareniacean species (Karenia brevis and Karlodinium veneficum) and Lepidodinium chlorophorum, and identified proteins involved in three plastid metabolic pathways synthesizing chlorophyll a (Chl a), heme and isoprene. The origins of the individual proteins of our interest were investigated, and we assessed how the three pathways were modified before and after the algal endosymbioses, which gave rise to the current non-canonical plastids. We observed a clear difference in the contribution of VI-type proteins across the three pathways. In both Karenia/Karlodinium and Lepidodinium, we observed a substantial contribution of VI-type proteins to the isoprene and heme biosynthesises. In sharp contrast, VI-type protein was barely detected in the Chl a biosynthesis in the three dinoflagellates.\\nDiscussion\\nPioneering works hypothesized that the ancestral kareniacean species had lost the photosynthetic activity prior to haptophyte endosymbiosis. The absence of VI-type proteins in the Chl a biosynthetic pathway in Karenia or Karlodinium is in good agreement with the putative non-photosynthetic nature proposed for their ancestor. The dominance of proteins with haptophyte origin in the Karenia/Karlodinium pathway suggests that their ancestor rebuilt the particular pathway by genes acquired from the endosymbiont. Likewise, we here propose that the ancestral Lepidodinium likely experienced a non-photosynthetic period and discarded the entire Chl a biosynthetic pathway prior to the green algal endosymbiosis. Nevertheless, Lepidodinium rebuilt the pathway by genes transferred from phylogenetically diverse organisms, rather than the green algal endosymbiont. We explore the reasons why green algal genes were barely utilized to reconstruct the Lepidodinium pathway.

Traditionally Cocholodinium and Gymnodinium sensu lato clade are distinguished based on the cingulum turn number, which has been increasingly recognized to be inadequate for Gymnodiniales genus classification. This has been improved by the combination of the apical groove characteristics and molecular phylogeny, which has led to the erection of several new genera (Takayama, Akashiwo, Karenia, and Karlodinium). Taking the apical groove characteristics and molecular phylogeny combined approach, we reexamined the historically taxonomically uncertain species Cochlodinium geminatum that formed massive blooms in Pearl River Estuary, China, in recent years. Samples were collected from a bloom in 2011 for morphological, characteristic pigment, and molecular analyses. We found that the cingulum in this species wraps around the cell body about 1.2 turns on average but can appear under the light microscopy to be >1.5 turns after the cells have been preserved. The shape of its apical groove, however, was stably an open-ended anticlockwise loop of kidney bean shape, similar to that of Polykrikos. Furthermore, the molecular phylogenetic analysis using 18S rRNA-ITS-28S rRNA gene cistron we obtained in this study also consistently placed this species closest to Polykrikos within the Gymnodinium sensu stricto clade and set it far separated from the clade of Cochlodinium. These results suggest that this species should be transferred to Polykrikos as Polykrikos geminatum. Our results reiterate the need to use the combination of apical groove morphology and molecular phylogeny for the classification of species within the genus of Cochlodinium and other Gymnodiniales lineages.