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Single cell genomics of uncultured marine alveolates shows paraphyly of basal dinoflagellates.

ISME J. 2018 01;12(1):304-308

Authors: Strassert JFH, Karnkowska A, Hehenberger E, Del Campo J, Kolisko M, Okamoto N, Burki F, Janouškovec J, Poirier C, Leonard G, Hallam SJ, Richards TA, Worden AZ, Santoro AE, Keeling PJ

Abstract
Marine alveolates (MALVs) are diverse and widespread early-branching dinoflagellates, but most knowledge of the group comes from a few cultured species that are generally not abundant in natural samples, or from diversity analyses of PCR-based environmental SSU rRNA gene sequences. To more broadly examine MALV genomes, we generated single cell genome sequences from seven individually isolated cells. Genes expected of heterotrophic eukaryotes were found, with interesting exceptions like presence of proteorhodopsin and vacuolar H+-pyrophosphatase. Phylogenetic analysis of concatenated SSU and LSU rRNA gene sequences provided strong support for the paraphyly of MALV lineages. Dinoflagellate viral nucleoproteins were found only in MALV groups that branched as sister to dinokaryotes. Our findings indicate that multiple independent origins of several characteristics early in dinoflagellate evolution, such as a parasitic life style, underlie the environmental diversity of MALVs, and suggest they have more varied trophic modes than previously thought.

PMID: 28994824 [PubMed – indexed for MEDLINE]

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Comparative Genomics of Color Morphs In the Coral Montastraea cavernosa.

Sci Rep. 2017 11 22;7(1):16039

Authors: Jarett JK, MacManes MD, Morrow KM, Pankey MS, Lesser MP

Abstract
Montastraea cavernosa is a common coral in the Caribbean basin found in several color morphs. To investigate the causes for brown and orange morphs we undertook a genomics approach on corals collected at the same time and depth in the Bahamas. The coral holobiont includes the host, symbiotic dinoflagellates (Symbiodinium spp.), and a diverse microbiome. While the coral host showed significant genetic differentiation between color morphs both the composition of the Symbiodinium spp. communities and the prokaryotic communities did not. Both targeted and global gene expression differences in the transcriptome of the host show no difference in fluorescent proteins while the metatranscriptome of the microbiome shows that pigments such as phycoerythrin and orange carotenoid protein of cyanobacterial origin are significantly greater in orange morphs, which is also consistent with the significantly greater number of cyanobacteria quantified by 16S rRNA reads and flow cytometry. The microbiome of orange color morphs expressed significantly more nitrogenase (nifH) transcripts consistent with their known ability to fix nitrogen. Both coral and Symbiodinium spp. transcriptomes from orange morphs had significantly increased expression of genes related to immune response and apoptosis, which may potentially be involved in maintaining and regulating the unique symbiont population in orange morphs.

PMID: 29167578 [PubMed – in process]

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The Plastid Genome in Cladophorales Green Algae Is Encoded by Hairpin Chromosomes.

Curr Biol. 2017 Dec 18;27(24):3771-3782.e6

Authors: Del Cortona A, Leliaert F, Bogaert KA, Turmel M, Boedeker C, Janouškovec J, Lopez-Bautista JM, Verbruggen H, Vandepoele K, De Clerck O

Abstract
Virtually all plastid (chloroplast) genomes are circular double-stranded DNA molecules, typically between 100 and 200 kb in size and encoding circa 80-250 genes. Exceptions to this universal plastid genome architecture are very few and include the dinoflagellates, where genes are located on DNA minicircles. Here we report on the highly deviant chloroplast genome of Cladophorales green algae, which is entirely fragmented into hairpin chromosomes. Short- and long-read high-throughput sequencing of DNA and RNA demonstrated that the chloroplast genes of Boodlea composita are encoded on 1- to 7-kb DNA contigs with an exceptionally high GC content, each containing a long inverted repeat with one or two protein-coding genes and conserved non-coding regions putatively involved in replication and/or expression. We propose that these contigs correspond to linear single-stranded DNA molecules that fold onto themselves to form hairpin chromosomes. The Boodlea chloroplast genes are highly divergent from their corresponding orthologs, and display an alternative genetic code. The origin of this highly deviant chloroplast genome most likely occurred before the emergence of the Cladophorales, and coincided with an elevated transfer of chloroplast genes to the nucleus. A chloroplast genome that is composed only of linear DNA molecules is unprecedented among eukaryotes, and highlights unexpected variation in plastid genome architecture.

PMID: 29199074 [PubMed – indexed for MEDLINE]

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Distribution and Evolution of Peroxisomes in Alveolates (Apicomplexa, Dinoflagellates, Ciliates).

Genome Biol Evol. 2018 01 01;10(1):1-13

Authors: Ludewig-Klingner AK, Michael V, Jarek M, Brinkmann H, Petersen J

Abstract
The peroxisome was the last organelle to be discovered and five decades later it is still the Cinderella of eukaryotic compartments. Peroxisomes have a crucial role in the detoxification of reactive oxygen species, the beta-oxidation of fatty acids, and the biosynthesis of etherphospholipids, and they are assumed to be present in virtually all aerobic eukaryotes. Apicomplexan parasites including the malaria and toxoplasmosis agents were described as the first group of mitochondriate protists devoid of peroxisomes. This study was initiated to reassess the distribution and evolution of peroxisomes in the superensemble Alveolata (apicomplexans, dinoflagellates, ciliates). We established transcriptome data from two chromerid algae (Chromera velia, Vitrella brassicaformis), and two dinoflagellates (Prorocentrum minimum, Perkinsus olseni) and identified the complete set of essential peroxins in all four reference species. Our comparative genome analysis provides unequivocal evidence for the presence of peroxisomes in Toxoplasma gondii and related genera. Our working hypothesis of a common peroxisomal origin of all alveolates is supported by phylogenetic analyses of essential markers such as the import receptor Pex5. Vitrella harbors the most comprehensive set of peroxisomal proteins including the catalase and the glyoxylate cycle and it is thus a promising model organism to investigate the functional role of this organelle in Apicomplexa.

PMID: 29202176 [PubMed – indexed for MEDLINE]

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Evidence for miRNA-mediated modulation of the host transcriptome in cnidarian-dinoflagellate symbiosis.

Mol Ecol. 2018 01;27(2):403-418

Authors: Baumgarten S, Cziesielski MJ, Thomas L, Michell CT, Esherick LY, Pringle JR, Aranda M, Voolstra CR

Abstract
Reef-building corals and other cnidarians living in symbiotic relationships with intracellular, photosynthetic dinoflagellates in the genus Symbiodinium undergo transcriptomic changes during infection with the algae and maintenance of the endosymbiont population. However, the precise regulatory mechanisms modulating the host transcriptome are unknown. Here, we report apparent post-transcriptional gene regulation by miRNAs in the sea anemone Aiptasia, a model system for cnidarian-dinoflagellate endosymbiosis. Aiptasia encodes mainly species-specific miRNAs, and there appears to have been recent differentiation within the Aiptasia genome of miRNAs that are commonly conserved among anthozoan cnidarians. Analysis of miRNA expression showed that both conserved and species-specific miRNAs are differentially expressed in response to endosymbiont infection. Using cross-linking immunoprecipitation of Argonaute, the central protein of the miRNA-induced silencing complex, we identified miRNA binding sites on a transcriptome-wide scale and found that the targets of the miRNAs regulated in response to symbiosis include genes previously implicated in biological processes related to Symbiodinium infection. Our study shows that cnidarian miRNAs recognize their mRNA targets via high-complementarity target binding and suggests that miRNA-mediated modulations of genes and pathways are important during the onset and maintenance of cnidarian-dinoflagellate endosymbiosis.

PMID: 29218749 [PubMed – indexed for MEDLINE]

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Comparative analysis of the genomes of Stylophora pistillata and Acropora digitifera provides evidence for extensive differences between species of corals.

Sci Rep. 2017 12 14;7(1):17583

Authors: Voolstra CR, Li Y, Liew YJ, Baumgarten S, Zoccola D, Flot JF, Tambutté S, Allemand D, Aranda M

Abstract
Stony corals form the foundation of coral reef ecosystems. Their phylogeny is characterized by a deep evolutionary divergence that separates corals into a robust and complex clade dating back to at least 245 mya. However, the genomic consequences and clade-specific evolution remain unexplored. In this study we have produced the genome of a robust coral, Stylophora pistillata, and compared it to the available genome of a complex coral, Acropora digitifera. We conducted a fine-scale gene-based analysis focusing on ortholog groups. Among the core set of conserved proteins, we found an emphasis on processes related to the cnidarian-dinoflagellate symbiosis. Genes associated with the algal symbiosis were also independently expanded in both species, but both corals diverged on the identity of ortholog groups expanded, and we found uneven expansions in genes associated with innate immunity and stress response. Our analyses demonstrate that coral genomes can be surprisingly disparate. Future analyses incorporating more genomic data should be able to determine whether the patterns elucidated here are not only characteristic of the differences between S. pistillata and A. digitifera but also representative of corals from the robust and complex clade at large.

PMID: 29242500 [PubMed – in process]

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Evolution: In Chloroplast Genomes, Anything Goes.

Curr Biol. 2017 12 18;27(24):R1305-R1307

Authors: Smith DR

Abstract
A new study shows that Cladophorales green algae have the most unconventional chloroplast DNAs ever observed, whereby genes are located on small linear single-stranded palindromic elements. This puzzling architecture has parallels with mini-circular chloroplast genomes of dinoflagellates and raises many questions about how it arose and is maintained.

PMID: 29257961 [PubMed – indexed for MEDLINE]

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6.0 K microarray reveals differential transcriptomic responses in the dinoflagellate Prorocentrum minimum exposed to polychlorinated biphenyl (PCB).

Chemosphere. 2018 Mar;195:398-409

Authors: Wang H, Guo R, Ki JS

Abstract
Endocrine disrupting chemicals (EDCs) have toxic effects on algae; however, their molecular genomic responses have not been sufficiently elucidated. Here, we evaluated genome-scaled responses of the dinoflagellate alga Prorocentrum minimum exposed to an EDC, polychlorinated biphenyl (PCB), using a 6.0 K microarray. Based on two-fold change cut-off, we identified that 609 genes (∼10.2%) responded to the PCB treatment. KEGG pathway analysis showed that differentially expressed genes (DEGs) were related to ribosomes, biosynthesis of amino acids, spliceosomes, and cellular processes. Many DEGs were involved in cell cycle progression, apoptosis, signal transduction, ion binding, and cellular transportation. In contrast, only a few genes related to photosynthesis and oxidative stress were expressed in response to PCB exposure. This was supported by that fact that there were no obvious changes in the photosynthetic efficiency and reactive oxygen species (ROS) production. These results suggest that PCB might not cause chloroplast and oxidative damage, but could lead to cell cycle arrest and apoptosis. In addition, various signal transduction and transport pathways might be disrupted in the cells, which could further contribute to cell death. These results expand the genomic understanding of the effects of EDCs on this dinoflagellate protist.

PMID: 29274579 [PubMed – indexed for MEDLINE]

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Time capsules in natural sediment archives-Tracking phytoplankton population genetic diversity and adaptation over multidecadal timescales in the face of environmental change.

Evol Appl. 2018 01;11(1):11-16

Authors: Ellegaard M, Godhe A, Ribeiro S

Abstract
Undisturbed records of resting stages produced in the past and stored in coastal sediments are very valuable to science, because they may provide unique insights into past evolutionary and ecological trajectories. Within marine phytoplankton, multidecadal time series of monoclonal strains germinated from resting stages have been established for diatoms (Skeletonema marinoi) and dinoflagellates (Pentapharsodinium dalei), spanning ca. a century. Phenotypic and genotypic analyses of these time series have revealed effects of past environmental changes on population genetic structure. Future perspectives include direct comparisons of phenotypes and genotypic data of populations, for example, by genomewide assays that can correlate phenotypic trends with genotypes and allele frequencies in temporally separated strains. Besides their usefulness as historical records, “seed” banks of phytoplankton resting stages also have the potential to provide an inoculum that influences present populations through “dispersal from the past” (the storage effect) and are important for adaptation to future environments through their standing genetic diversity.

PMID: 29302268 [PubMed]

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Genetic transformation of cell-walled plant and algae cells: delivering DNA through the cell wall.

Brief Funct Genomics. 2018 01 01;17(1):26-33

Authors: Ortiz-Matamoros MF, Villanueva MA, Islas-Flores T

Abstract
Transformation techniques are a fundamental tool for functional genomics studies. These techniques are routinely used in many prokaryotic and eukaryotic organisms, but in eukaryotes that are surrounded by a cell wall, these protocols have proven difficult to successfully deliver heterologous or homologous DNA within their cytoplasm and nucleus. Such cell-walled organisms represent a challenge that requires the development of genetic transformation techniques that are able to overcome their natural barrier, to achieve targeted gene expression. Here, we review the techniques that have been proven successful and applied to these cell-walled eukaryotic organisms. We focus, especially, on plant cells, microalgae, and the latest approaches to mediate DNA uptake by the photosynthetic dinoflagellate Symbiodinium.

PMID: 29365068 [PubMed – indexed for MEDLINE]