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Patrick J. Keeling - One of the best experts on this subject based on the ideXlab platform.

  • a kleptoPlastidic dinoflagellate and the tipping point between transient and fully integrated Plastid endosymbiosis
    Proceedings of the National Academy of Sciences of the United States of America, 2019
    Co-Authors: Elisabeth Hehenberger, Rebecca J Gast, Patrick J. Keeling
    Abstract:

    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.

  • a common red algal origin of the apicomplexan dinoflagellate and heterokont Plastids
    Proceedings of the National Academy of Sciences of the United States of America, 2010
    Co-Authors: Jan Janouskovec, Ales Horak, Miroslav Obornik, Julius Lukes, Patrick J. Keeling
    Abstract:

    The discovery of a nonphotosynthetic Plastid in malaria and other apicomplexan parasites has sparked a contentious debate about its evolutionary origin. Molecular data have led to conflicting conclusions supporting either its green algal origin or red algal origin, perhaps in common with the Plastid of related dinoflagellates. This distinction is critical to our understanding of apicomplexan evolution and the evolutionary history of endosymbiosis and photosynthesis; however, the two Plastids are nearly impossible to compare due to their nonoverlapping information content. Here we describe the complete Plastid genome sequences and Plastid-associated data from two independent photosynthetic lineages represented by Chromera velia and an undescribed alga CCMP3155 that we show are closely related to apicomplexans. These Plastids contain a suite of features retained in either apicomplexan (four Plastid membranes, the ribosomal superoperon, conserved gene order) or dinoflagellate Plastids (form II Rubisco acquired by horizontal transfer, transcript polyuridylylation, thylakoids stacked in triplets) and encode a full collective complement of their reduced gene sets. Together with whole Plastid genome phylogenies, these characteristics provide multiple lines of evidence that the extant Plastids of apicomplexans and dinoflagellates were inherited by linear descent from a common red algal endosymbiont. Our phylogenetic analyses also support their close relationship to Plastids of heterokont algae, indicating they all derive from the same endosymbiosis. Altogether, these findings support a relatively simple path of linear descent for the evolution of photosynthesis in a large proportion of algae and emphasize Plastid loss in several lineages (e.g., ciliates, Cryptosporidium, and Phytophthora).

  • complete nucleotide sequence of the chlorarachniophyte nucleomorph nature s smallest nucleus
    Proceedings of the National Academy of Sciences of the United States of America, 2006
    Co-Authors: Paul R. Gilson, Claudio H. Slamovits, Vanessa Su, Michael Reith, Patrick J. Keeling, Geoffrey I Mcfadden
    Abstract:

    The introduction of Plastids into different heterotrophic protists created lineages of algae that diversified explosively, proliferated in marine and freshwater environments, and radically altered the biosphere. The origins of these secondary Plastids are usually inferred from the presence of additional Plastid membranes. However, two examples provide unique snapshots of secondary-endosymbiosis-in-action, because they retain a vestige of the endosymbiont nucleus known as the nucleomorph. These are chlorarachniophytes and cryptomonads, which acquired their Plastids from a green and red alga respectively. To allow comparisons between them, we have sequenced the nucleomorph genome from the chlorarachniophyte Bigelowiella natans: at a mere 373,000 bp and with only 331 genes, the smallest nuclear genome known and a model for extreme reduction. The genome is eukaryotic in nature, with three linear chromosomes containing densely packed genes with numerous overlaps. The genome is replete with 852 introns, but these are the smallest introns known, being only 18, 19, 20, or 21 nt in length. These pygmy introns are shown to be miniaturized versions of normal-sized introns present in the endosymbiont at the time of capture. Seventeen nucleomorph genes encode proteins that function in the Plastid. The other nucleomorph genes are housekeeping entities, presumably underpinning maintenance and expression of these Plastid proteins. Chlorarachniophyte Plastids are thus serviced by three different genomes (Plastid, nucleomorph, and host nucleus) requiring remarkable coordination and targeting. Although originating by two independent endosymbioses, chlorarachniophyte and cryptomonad nucleomorph genomes have converged upon remarkably similar architectures but differ in many molecular details that reflect two distinct trajectories to hypercompaction and reduction.

  • Complete nucleotide sequence of the chlorarachniophyte nucleomorph: Nature’s smallest nucleus
    Proceedings of the National Academy of Sciences of the United States of America, 2006
    Co-Authors: Paul R. Gilson, Claudio H. Slamovits, Michael Reith, Patrick J. Keeling, Geoffrey I Mcfadden
    Abstract:

    The introduction of Plastids into different heterotrophic protists created lineages of algae that diversified explosively, proliferated in marine and freshwater environments, and radically altered the biosphere. The origins of these secondary Plastids are usually inferred from the presence of additional Plastid membranes. However, two examples provide unique snapshots of secondary-endosymbiosis-in-action, because they retain a vestige of the endosymbiont nucleus known as the nucleomorph. These are chlorarachniophytes and cryptomonads, which acquired their Plastids from a green and red alga respectively. To allow comparisons between them, we have sequenced the nucleomorph genome from the chlorarachniophyte Bigelowiella natans: at a mere 373,000 bp and with only 331 genes, the smallest nuclear genome known and a model for extreme reduction. The genome is eukaryotic in nature, with three linear chromosomes containing densely packed genes with numerous overlaps. The genome is replete with 852 introns, but these are the smallest introns known, being only 18, 19, 20, or 21 nt in length. These pygmy introns are shown to be miniaturized versions of normal-sized introns present in the endosymbiont at the time of capture. Seventeen nucleomorph genes encode proteins that function in the Plastid. The other nucleomorph genes are housekeeping entities, presumably underpinning maintenance and expression of these Plastid proteins. Chlorarachniophyte Plastids are thus serviced by three different genomes (Plastid, nucleomorph, and host nucleus) requiring remarkable coordination and targeting. Although originating by two independent endosymbioses, chlorarachniophyte and cryptomonad nucleomorph genomes have converged upon remarkably similar architectures but differ in many molecular details that reflect two distinct trajectories to hypercompaction and reduction.

  • a tertiary Plastid uses genes from two endosymbionts
    Journal of Molecular Biology, 2006
    Co-Authors: Nicola J Patron, Ross F. Waller, Patrick J. Keeling
    Abstract:

    The origin and subsequent spread of Plastids by endosymbiosis had a major environmental impact and altered the course of a great proportion of eukaryotic biodiversity. The ancestor of dinoflagellates contained a secondary Plastid that was acquired in an ancient endosymbiotic event, where a eukaryotic cell engulfed a red alga. This is known as secondary endosymbiosis and has happened several times in eukaryotic evolution. Certain dinoflagellates, however, are unique in having replaced this secondary Plastid in an additional (tertiary) round of endosymbiosis. Most Plastid proteins are encoded in the nucleus of the host and are targeted to the organelle. When secondary or tertiary endosymbiosis takes place, it is thought that these genes move from nucleus to nucleus, so the Plastid retains the same proteome. We have conducted large-scale expressed sequence tag (EST) surveys from Karlodinium micrum, a dinoflagellate with a tertiary haptophyte-derived Plastid, and two haptophytes, Isochrysis galbana and Pavlova lutheri. We have identified all Plastid-targeted proteins, analysed the phylogenetic origin of each protein, and compared their Plastid-targeting transit peptides. Many Plastid-targeted genes in the Karlodinium nucleus are indeed of haptophyte origin, but some genes were also retained from the original Plastid (showing the two Plastids likely co-existed in the same cell), in other cases multiple isoforms of different origins exist. We analysed Plastid-targeting sequences and found the transit peptides in K. micrum are different from those found in either dinoflagellates or haptophytes, pointing to a Plastid with an evolutionarily chimeric proteome, and a massive remodelling of protein trafficking during Plastid replacement.

Claire Jubin - One of the best experts on this subject based on the ideXlab platform.

  • Plastid genomes of two brown algae ectocarpus siliculosus and fucus vesiculosus further insights on the evolution of red algal derived Plastids
    BMC Evolutionary Biology, 2009
    Co-Authors: Gildas Le Corguille, Gareth A Pearson, Marta Valente, Carla Viegas, Bernhard Gschloessl, Erwan Corre, Xavier Bailly, Akira F Peters, Claire Jubin
    Abstract:

    Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived Plastids. The chromalveolate hypothesis proposes that the red-algal derived Plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and Plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for phylogenetic reconstruction but insufficient sequence data have been available for red-algal derived Plastid genomes. The chloroplast genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus, have been fully sequenced. These species represent two distinct orders of the Phaeophyceae, which is a major group within the heterokont lineage. The sizes of the circular Plastid genomes are 139,954 and 124,986 base pairs, respectively, the size difference being due principally to the presence of longer inverted repeat and intergenic regions in E. siliculosus. Gene contents of the two Plastids are similar with 139-148 protein-coding genes, 28-31 tRNA genes, and 3 ribosomal RNA genes. The two genomes also exhibit very similar rearrangements compared to other sequenced Plastid genomes. The tRNA-Leu gene of E. siliculosus lacks an intron, in contrast to the F. vesiculosus and other heterokont Plastid homologues, suggesting its recent loss in the Ectocarpales. Most of the brown algal Plastid genes are shared with other red-algal derived Plastid genomes, but a few are absent from raphidophyte or diatom Plastid genomes. One of these regions is most similar to an apicomplexan nuclear sequence. The phylogenetic relationship between heterokonts, cryptophytes and haptophytes (collectively referred to as chromists) Plastids was investigated using several datasets of concatenated proteins from two cyanobacterial genomes and 18 Plastid genomes, including most of the available red algal and chromist Plastid genomes. The phylogenetic studies using concatenated Plastid proteins still do not resolve the question of the monophyly of all chromist Plastids. However, these results support both the monophyly of heterokont Plastids and that of cryptophyte and haptophyte Plastids, in agreement with nuclear phylogenies.

  • Plastid genomes of two brown algae ectocarpus siliculosus and fucus vesiculosus further insights on the evolution of red algal derived Plastids
    BMC Evolutionary Biology, 2009
    Co-Authors: Gildas Le Corguille, Gareth A Pearson, Marta Valente, Carla Viegas, Bernhard Gschloessl, Erwan Corre, Xavier Bailly, Akira F Peters, Claire Jubin, Benoit Vacherie
    Abstract:

    Background Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived Plastids. The chromalveolate hypothesis proposes that the red-algal derived Plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and Plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for phylogenetic reconstruction but insufficient sequence data have been available for red-algal derived Plastid genomes.

Ralph Bock - One of the best experts on this subject based on the ideXlab platform.

  • chloroplast competition is controlled by lipid biosynthesis in evening primroses
    Proceedings of the National Academy of Sciences of the United States of America, 2019
    Co-Authors: Johanna Sobanski, Patrick Giavalisco, Axel Fischer, Dirk Walther, Mark Aurel Schottler, Tommaso Pellizzer, Hieronim Golczyk, Toshihiro Obata, Julia M Kreiner, Ralph Bock
    Abstract:

    In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast-replicating or aggressive chloroplasts (Plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of Plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the Plastid genome of the evening primrose Oenothera . Repeats in the regulatory region of accD (the Plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate-limiting step of lipid biosynthesis), as well as in ycf2 (a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of Plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the Plastid envelope membrane. These in turn determine Plastid division and/or turnover rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, as Plastid competitiveness can result in uniparental inheritance (through elimination of the “weak” Plastid) or biparental inheritance (when two similarly “strong” Plastids are transmitted).

  • chloroplast competition is controlled by lipid biosynthesis in evening primroses
    bioRxiv, 2018
    Co-Authors: Johanna Sobanski, Patrick Giavalisco, Axel Fischer, Dirk Walther, Mark Aurel Schottler, Tommaso Pellizzer, Hieronim Golczyk, Toshihiro Obata, Julia M Kreiner, Ralph Bock
    Abstract:

    In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast replicating or aggressive chloroplasts (Plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of Plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the Plastid genome of the evening primrose Oenothera. Repeats in the regulatory region of accD (the Plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate limiting step of lipid biosynthesis), as well as in ycf2 (a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of Plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the Plastid envelope membrane. These in turn determine Plastid division and/or turn-over rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, since Plastid competitiveness can result in uniparental inheritance (through elimination of the 9weak9 Plastid) or biparental inheritance (when two similarly 9strong9 Plastids are transmitted).

  • biparental inheritance of chloroplasts is controlled by lipid biosynthesis in evening primroses
    bioRxiv, 2018
    Co-Authors: Johanna Sobanski, Patrick Giavalisco, Axel Fischer, Dirk Walther, Mark Aurel Schottler, Tommaso Pellizzer, Hieronim Golczyk, Toshihiro Obata, Ralph Bock, Barbara B Sears
    Abstract:

    In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but the reasons underlying this fundamental biological principle are far from being understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of selfish cytoplasmic elements. Those can be, for example, fast replicating chloroplasts (Plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show, that Plastid competition is a metabolic phenotype determined by extremely rapidly evolving regions in the Plastid genome of the evening primrose Oenothera. Polymorphisms in repeats of the regulatory region of accD (the Plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first step of lipid biosynthesis), are responsible for the differences in competitive behavior of different Plastid genotypes. These cytoplasmic drive loci change lipid synthesis and most likely lipid profiles of the Plastid envelope membrane. Consequently, this determines Plastid division and/or turn-over rates and hence competitiveness. Since Plastid competition can result in uniparental inheritance (through elimination of the 9weak9 Plastid) or biparental inheritance (when two similarly 9strong9 Plastids are transmitted), this work uncovers for the first time a genetic determinant of organelle inheritance.

  • biparental inheritance of chloroplasts is controlled by lipid biosynthesis
    bioRxiv, 2018
    Co-Authors: Johanna Sobanski, Patrick Giavalisco, Axel Fischer, Dirk Walther, Mark Aurel Schottler, Tommaso Pellizzer, Hieronim Golczyk, Toshihiro Obata, Ralph Bock, Barbara B Sears
    Abstract:

    In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but the reasons underlying this fundamental biological principle are far from being understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of selfish cytoplasmic elements. Those can be, for example, fast replicating chloroplasts (Plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show, that Plastid competition is a metabolic phenotype determined by extremely rapidly evolving regions in the Plastid genome of the evening primrose Oenothera. Polymorphisms in repeats of the regulatory region of accD (the only Plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first step of lipid biosynthesis), are responsible for the differences in competitive behavior of different Plastid genotypes. These cytoplasmic drive loci change lipid synthesis and consequently lipid profiles of the Plastid envelope membrane. This most likely determines Plastid division and/or turn-over rates and hence competitiveness. Since Plastid competition can result in uniparental inheritance (through elimination of the 9weak9 Plastid) or biparental inheritance (when two similarly 9strong9 Plastids are transmitted), this work uncovers for the first time a genetic determinant of organelle inheritance.

  • the translational apparatus of Plastids and its role in plant development
    Molecular Plant, 2014
    Co-Authors: Nadine Tiller, Ralph Bock
    Abstract:

    Chloroplasts (Plastids) possess a genome and their own machinery to express it. Translation in Plastids occurs on bacterial-type 70S ribosomes utilizing a set of tRNAs that is entirely encoded in the Plastid genome. In recent years, the components of the chloroplast translational apparatus have been intensely studied by proteomic approaches and by reverse genetics in the model systems tobacco (Plastid-encoded components) and Arabidopsis (nucleus-encoded components). This work has provided important new insights into the structure, function, and biogenesis of chloroplast ribosomes, and also has shed fresh light on the molecular mechanisms of the translation process in Plastids. In addition, mutants affected in Plastid translation have yielded strong genetic evidence for chloroplast genes and gene products influencing plant development at various levels, presumably via retrograde signaling pathway(s). In this review, we describe recent progress with the functional analysis of components of the chloroplast translational machinery and discuss the currently available evidence that supports a significant impact of Plastid translational activity on plant anatomy and morphology.

Geoffrey I Mcfadden - One of the best experts on this subject based on the ideXlab platform.

  • isolating the plasmodium falciparum apicoplast using magnetic beads
    Methods of Molecular Biology, 2018
    Co-Authors: Cyrille Y Botté, Geoffrey I Mcfadden, Yoshiki Yamaryobotte
    Abstract:

    Plastids are key organelles in both photosynthetic and nonphotosynthetic organisms. In photosynthetic organisms, Plastids can be readily purified using differential centrifugations due to the high density of photosynthetic membranes or thylakoids. The apicomplexan Plastid (the apicoplast) is an essential nonphotosynthetic Plastid that lacks thylakoid and was not readily purified using conventional methods. Here, we describe a tractable method to purify intact apicoplasts from Plasmodium falciparum blood stages using magnetic beads and affinity purification.

  • endosymbiosis undone by stepwise elimination of the Plastid in a parasitic dinoflagellate
    Proceedings of the National Academy of Sciences of the United States of America, 2015
    Co-Authors: James I Macrae, Sebastian G Gornik, Andrew Cassin, Abhinay Ramaprasad, Zineb Rchiad, Malcolm J Mcconville, Antony Bacic, Geoffrey I Mcfadden
    Abstract:

    Organelle gain through endosymbiosis has been integral to the origin and diversification of eukaryotes, and, once gained, Plastids and mitochondria seem seldom lost. Indeed, discovery of nonphotosynthetic Plastids in many eukaryotes—notably, the apicoplast in apicomplexan parasites such as the malaria pathogen Plasmodium—highlights the essential metabolic functions performed by Plastids beyond photosynthesis. Once a cell becomes reliant on these ancillary functions, organelle dependence is apparently difficult to overcome. Previous examples of endosymbiotic organelle loss (either mitochondria or Plastids), which have been invoked to explain the origin of eukaryotic diversity, have subsequently been recognized as organelle reduction to cryptic forms, such as mitosomes and apicoplasts. Integration of these ancient symbionts with their hosts has been too well developed to reverse. Here, we provide evidence that the dinoflagellate Hematodinium sp., a marine parasite of crustaceans, represents a rare case of endosymbiotic organelle loss by the elimination of the Plastid. Extensive RNA and genomic sequencing data provide no evidence for a Plastid organelle, but, rather, reveal a metabolic decoupling from known Plastid functions that typically impede organelle loss. This independence has been achieved through retention of ancestral anabolic pathways, enzyme relocation from the Plastid to the cytosol, and metabolic scavenging from the parasite’s host. Hematodinium sp. thus represents a further dimension of endosymbiosis—life after the organelle.

  • complete nucleotide sequence of the chlorarachniophyte nucleomorph nature s smallest nucleus
    Proceedings of the National Academy of Sciences of the United States of America, 2006
    Co-Authors: Paul R. Gilson, Claudio H. Slamovits, Vanessa Su, Michael Reith, Patrick J. Keeling, Geoffrey I Mcfadden
    Abstract:

    The introduction of Plastids into different heterotrophic protists created lineages of algae that diversified explosively, proliferated in marine and freshwater environments, and radically altered the biosphere. The origins of these secondary Plastids are usually inferred from the presence of additional Plastid membranes. However, two examples provide unique snapshots of secondary-endosymbiosis-in-action, because they retain a vestige of the endosymbiont nucleus known as the nucleomorph. These are chlorarachniophytes and cryptomonads, which acquired their Plastids from a green and red alga respectively. To allow comparisons between them, we have sequenced the nucleomorph genome from the chlorarachniophyte Bigelowiella natans: at a mere 373,000 bp and with only 331 genes, the smallest nuclear genome known and a model for extreme reduction. The genome is eukaryotic in nature, with three linear chromosomes containing densely packed genes with numerous overlaps. The genome is replete with 852 introns, but these are the smallest introns known, being only 18, 19, 20, or 21 nt in length. These pygmy introns are shown to be miniaturized versions of normal-sized introns present in the endosymbiont at the time of capture. Seventeen nucleomorph genes encode proteins that function in the Plastid. The other nucleomorph genes are housekeeping entities, presumably underpinning maintenance and expression of these Plastid proteins. Chlorarachniophyte Plastids are thus serviced by three different genomes (Plastid, nucleomorph, and host nucleus) requiring remarkable coordination and targeting. Although originating by two independent endosymbioses, chlorarachniophyte and cryptomonad nucleomorph genomes have converged upon remarkably similar architectures but differ in many molecular details that reflect two distinct trajectories to hypercompaction and reduction.

  • Complete nucleotide sequence of the chlorarachniophyte nucleomorph: Nature’s smallest nucleus
    Proceedings of the National Academy of Sciences of the United States of America, 2006
    Co-Authors: Paul R. Gilson, Claudio H. Slamovits, Michael Reith, Patrick J. Keeling, Geoffrey I Mcfadden
    Abstract:

    The introduction of Plastids into different heterotrophic protists created lineages of algae that diversified explosively, proliferated in marine and freshwater environments, and radically altered the biosphere. The origins of these secondary Plastids are usually inferred from the presence of additional Plastid membranes. However, two examples provide unique snapshots of secondary-endosymbiosis-in-action, because they retain a vestige of the endosymbiont nucleus known as the nucleomorph. These are chlorarachniophytes and cryptomonads, which acquired their Plastids from a green and red alga respectively. To allow comparisons between them, we have sequenced the nucleomorph genome from the chlorarachniophyte Bigelowiella natans: at a mere 373,000 bp and with only 331 genes, the smallest nuclear genome known and a model for extreme reduction. The genome is eukaryotic in nature, with three linear chromosomes containing densely packed genes with numerous overlaps. The genome is replete with 852 introns, but these are the smallest introns known, being only 18, 19, 20, or 21 nt in length. These pygmy introns are shown to be miniaturized versions of normal-sized introns present in the endosymbiont at the time of capture. Seventeen nucleomorph genes encode proteins that function in the Plastid. The other nucleomorph genes are housekeeping entities, presumably underpinning maintenance and expression of these Plastid proteins. Chlorarachniophyte Plastids are thus serviced by three different genomes (Plastid, nucleomorph, and host nucleus) requiring remarkable coordination and targeting. Although originating by two independent endosymbioses, chlorarachniophyte and cryptomonad nucleomorph genomes have converged upon remarkably similar architectures but differ in many molecular details that reflect two distinct trajectories to hypercompaction and reduction.

Gildas Le Corguille - One of the best experts on this subject based on the ideXlab platform.

  • Plastid genomes of two brown algae ectocarpus siliculosus and fucus vesiculosus further insights on the evolution of red algal derived Plastids
    BMC Evolutionary Biology, 2009
    Co-Authors: Gildas Le Corguille, Gareth A Pearson, Marta Valente, Carla Viegas, Bernhard Gschloessl, Erwan Corre, Xavier Bailly, Akira F Peters, Claire Jubin
    Abstract:

    Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived Plastids. The chromalveolate hypothesis proposes that the red-algal derived Plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and Plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for phylogenetic reconstruction but insufficient sequence data have been available for red-algal derived Plastid genomes. The chloroplast genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus, have been fully sequenced. These species represent two distinct orders of the Phaeophyceae, which is a major group within the heterokont lineage. The sizes of the circular Plastid genomes are 139,954 and 124,986 base pairs, respectively, the size difference being due principally to the presence of longer inverted repeat and intergenic regions in E. siliculosus. Gene contents of the two Plastids are similar with 139-148 protein-coding genes, 28-31 tRNA genes, and 3 ribosomal RNA genes. The two genomes also exhibit very similar rearrangements compared to other sequenced Plastid genomes. The tRNA-Leu gene of E. siliculosus lacks an intron, in contrast to the F. vesiculosus and other heterokont Plastid homologues, suggesting its recent loss in the Ectocarpales. Most of the brown algal Plastid genes are shared with other red-algal derived Plastid genomes, but a few are absent from raphidophyte or diatom Plastid genomes. One of these regions is most similar to an apicomplexan nuclear sequence. The phylogenetic relationship between heterokonts, cryptophytes and haptophytes (collectively referred to as chromists) Plastids was investigated using several datasets of concatenated proteins from two cyanobacterial genomes and 18 Plastid genomes, including most of the available red algal and chromist Plastid genomes. The phylogenetic studies using concatenated Plastid proteins still do not resolve the question of the monophyly of all chromist Plastids. However, these results support both the monophyly of heterokont Plastids and that of cryptophyte and haptophyte Plastids, in agreement with nuclear phylogenies.

  • Plastid genomes of two brown algae ectocarpus siliculosus and fucus vesiculosus further insights on the evolution of red algal derived Plastids
    BMC Evolutionary Biology, 2009
    Co-Authors: Gildas Le Corguille, Gareth A Pearson, Marta Valente, Carla Viegas, Bernhard Gschloessl, Erwan Corre, Xavier Bailly, Akira F Peters, Claire Jubin, Benoit Vacherie
    Abstract:

    Background Heterokont algae, together with cryptophytes, haptophytes and some alveolates, possess red-algal derived Plastids. The chromalveolate hypothesis proposes that the red-algal derived Plastids of all four groups have a monophyletic origin resulting from a single secondary endosymbiotic event. However, due to incongruence between nuclear and Plastid phylogenies, this controversial hypothesis remains under debate. Large-scale genomic analyses have shown to be a powerful tool for phylogenetic reconstruction but insufficient sequence data have been available for red-algal derived Plastid genomes.