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Debashish Bhattacharya - One of the best experts on this subject based on the ideXlab platform.
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The Algal Tree of Life from a Genomics Perspective
Photosynthesis in Algae: Biochemical and Physiological Mechanisms, 2020Co-Authors: Debashish Bhattacharya, Dana C. PriceAbstract:It is now widely recognized that photosynthetic eukaryotes (algae and plants) have polyphyletic origins in the eukaryotic tree of life (ETOL). The primary endosymbiosis that gave rise to the first photosynthetic organelle (plastid) occurred ca. 1.6 billion years ago via the capture and retention of a free-living cyanobacterium by a single-celled protist. This proto-alga is the ancestor of the Archaeplastida that includes the photosynthetic glaucophytes, red algae, and the green lineage. The Archaeplastida plastid spread into other protist lineages through serial endosymbiosis, giving rise to dominant marine phytoplankton such as diatoms and dinoflagellates. A significant effort has been expended on elucidating plastid origin, function, and its impacts on global primary productivity and geochemical cycles. Here we focus on the placement of algae in the ETOL, with particular emphasis on the major groups: Archaeplastida, SAR (stramenopiles, alveolates, rhizarians), haptophytes, and cryptophytes. Our approach is to rely on the analysis of ortholog groups identified in recently generated genomic and transcriptomic data to infer the ETOL, rather than using a subset of manually chosen and curated genes. We show that bioinformatic pipelines effectively, and with minimal curation recover a robust ETOL, when compared to the classical approach of utilizing “designer datasets” in multiple analyses.
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Paulinella, a model for understanding plastid primary endosymbiosis.
Journal of Phycology, 2020Co-Authors: Arwa Gabr, Arthur R. Grossman, Debashish BhattacharyaAbstract:The uptake and conversion of a free-living cyanobacterium into a photosynthetic organelle by the single-celled Archaeplastida ancestor helped transform the biosphere from low to high oxygen. There are two documented, independent cases of plastid primary endosymbiosis. The first is the well-studied instance in Archaeplastida that occurred ca. 1.6 billion years ago, whereas the second occurred 90-140 million years ago, establishing a permanent photosynthetic compartment (the chromatophore) in amoebae in the genus Paulinella. Here, we briefly summarize knowledge about plastid origin in the Archaeplastida and then focus on Paulinella. In particular, we describe features of the Paulinella chromatophore that make it a model for examining earlier events in the evolution of photosynthetic organelles. Our review stresses recently gained insights into the evolution of chromatophore and nuclear encoded DNA sequences in Paulinella, metabolic connectivity between the endosymbiont and cytoplasm, and systems that target proteins into the chromatophore. We also describe future work with Paulinella, and the potential rewards and challenges associated with developing further this model system.
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Kingdom-wide Comparison Reveals the Evolution of Diurnal Gene Expression in Archaeplastida
Nature communications, 2019Co-Authors: Camilla Ferrari, Dana C. Price, Debashish Bhattacharya, Sebastian Proost, Marcin Janowski, Zoran Nikoloski, Takayuki Tohge, Arren Bar-even, Jörg D. Becker, Alisdair FernieAbstract:Plants have adapted to the diurnal light-dark cycle by establishing elaborate transcriptional programs that coordinate many metabolic, physiological, and developmental responses to the external environment. These transcriptional programs have been studied in only a few species, and their function and conservation across algae and plants is currently unknown. We performed a comparative transcriptome analysis of the diurnal cycle of nine members of Archaeplastida, and we observed that, despite large phylogenetic distances and dramatic differences in morphology and lifestyle, diurnal transcriptional programs of these organisms are similar. Expression of genes related to cell division and the majority of biological pathways depends on the time of day in unicellular algae but we did not observe such patterns at the tissue level in multicellular land plants. Hence, our study provides evidence for the universality of diurnal gene expression and elucidates its evolutionary history among different photosynthetic eukaryotes.
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Kingdom-wide comparison reveals the evolution of diurnal gene expression in Archaeplastida
Nature Publishing Group, 2019Co-Authors: Camilla Ferrari, Debashish Bhattacharya, Sebastian Proost, Marcin Janowski, Jörg Becker, Zoran Nikoloski, Dana Price, Takayuki Tohge, Arren Bar-even, Alisdair FernieAbstract:The diurnal cycle exerts influences on various aspects of plant biology. Here, the authors generate and compare diurnal transcriptomics data from nine members of Archaeplastida representing major clades
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Host-pathogen biotic interactions shaped vitamin K metabolism in Archaeplastida
Scientific reports, 2018Co-Authors: Ugo Cenci, Christophe Colleoni, Derifa Kadouche, Hongyu Qiu, Trestan Pillonel, Pierre Cardol, Claire Remacle, Malika Chabi, Gilbert Greub, Debashish BhattacharyaAbstract:Menaquinone (vitamin K2) shuttles electrons between membrane-bound respiratory complexes under microaerophilic conditions. In photosynthetic eukaryotes and cyanobacteria, phylloquinone (vitamin K1) participates in photosystem I function. Here we elucidate the evolutionary history of vitamin K metabolism in algae and plants. We show that Chlamydiales intracellular pathogens made major genetic contributions to the synthesis of the naphthoyl ring core and the isoprenoid side-chain of these quinones. Production of the core in extremophilic red algae is under control of a menaquinone (Men) gene cluster consisting of 7 genes that putatively originated via lateral gene transfer (LGT) from a chlamydial donor to the plastid genome. In other green and red algae, functionally related nuclear genes also originated via LGT from a non-cyanobacterial, albeit unidentified source. In addition, we show that 3–4 of the 9 required steps for synthesis of the isoprenoid side chains are under control of genes of chlamydial origin. These results are discussed in the light of the hypoxic response experienced by the cyanobacterial endosymbiont when it gained access to the eukaryotic cytosol.
Steven G Ball - One of the best experts on this subject based on the ideXlab platform.
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Analysis of an improved Cyanophora paradoxa genome assembly.
DNA Research, 2019Co-Authors: Dana C. Price, Ursula Goodenough, Camilla Ferrari, Fabio Facchinelli, Marek Mutwil, Robyn Roth, Thamali Kariyawasam, Steven G Ball, Ugo CenciAbstract:Glaucophyta are members of the Archaeplastida, the founding group of photosynthetic eukaryotes that also includes red algae (Rhodophyta), green algae, and plants (Viridiplantae). Here we present a high-quality assembly, built using long-read sequences, of the ca. 100 Mb nuclear genome of the model glaucophyte Cyanophora paradoxa. We also conducted a quick-freeze deep-etch electron microscopy (QFDEEM) analysis of C. paradoxa cells to investigate glaucophyte morphology in comparison to other organisms. Using the genome data, we generated a resolved 115-taxon eukaryotic tree of life that includes a well-supported, monophyletic Archaeplastida. Analysis of muroplast peptidoglycan (PG) ultrastructure using QFDEEM shows that PG is most dense at the cleavage-furrow. Analysis of the chlamydial contribution to glaucophytes and other Archaeplastida shows that these foreign sequences likely played a key role in anaerobic glycolysis in primordial algae to alleviate ATP starvation under night-time hypoxia. The robust genome assembly of C. paradoxa significantly advances knowledge about this model species and provides a reference for exploring the panoply of traits associated with the anciently diverged glaucophyte lineage.
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was the chlamydial adaptative strategy to tryptophan starvation an early determinant of plastid endosymbiosis
Frontiers in Cellular and Infection Microbiology, 2016Co-Authors: Ugo Cenci, Christophe Colleoni, Mathieu Ducatez, Derifa Kadouche, Steven G BallAbstract:Chlamydiales were recently proposed to have sheltered the future cyanobacterial ancestor of plastids in a common inclusion. The intracellular pathogens are thought to have donated those critical transporters that triggered the efflux of photosynthetic carbon and the consequent onset of symbiosis. Chlamydiales are also suspected to have encoded glycogen metabolism TTS (Type Three Secretion) effectors responsible for photosynthetic carbon assimilation in the eukaryotic cytosol. We now review the reasons underlying other chlamydial lateral gene transfers (LGT) evidenced in the descendants of plastid endosymbiosis. In particular, we show that half of the genes encoding enzymes of tryptophan synthesis in Archaeplastida are of chlamydial origin. Tryptophan is known to define an essential cue triggering two alternative modes of replication in Chlamydiales. In addition, sophisticated tryptophan starvation mechanisms are known to have been implemented as antibacterial defenses by their eukaryotic hosts. We propose that Chlamydiales have donated their tryptophan operon to the emerging plastid to ensure increased synthesis of tryptophan by the plastid ancestor. This would have allowed massive expression of the tryptophan rich chlamydial transporters responsible for symbiosis. It would also have allowed possible export of this valuable amino-acid in the inclusion of the tryptophan hungry pathogens. Free-living single cell cyanobacteria are devoid of proteins able to transport this amino-acid. We therefore investigated the phylogeny of the E.coli Tyr/Trp transporters and found yet another LGT from Chlamydiales to Archaeplastida thereby considerably strengthening our proposal.
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Commentary: Plastid establishment did not require a chlamydial partner.
Frontiers in cellular and infection microbiology, 2016Co-Authors: Steven G Ball, Debashish Bhattacharya, Huan Qiu, Andreas P. M. WeberAbstract:Several groups have independently proposed an active role for Chlamydiales in primary plastid establishment in Archaeplastida (Huang and Gogarten, 2007; Becker et al., 2008; Moustafa et al., 2008). We relied on a combination of biochemical and phylogenetic evidence to erect the MAT (Menage a Trois) hypothesis (Ball et al., 2013; Facchinelli et al., 2013). Under this scenario, Chlamydiales sheltered the once free-living cyanobacterial plastid ancestor from host defenses and provided critical components such as carbohydrate transporters and protein effectors that allowed the storage of exported carbohydrates into host glycogen pools. A recent paper by Domman et al. (2015) reassessed the phylogenies published by us and others on these components. These authors applied evolutionary models that better account for across-site and across-branch sequence compositional variation (i.e., Bayesian approaches with the CAT family of evolutionary models Lartillot and Philippe, 2004) to reanalyze proteins involved in glycogen metabolism. These are either chlamydial effectors (GlgC, ADP-glucose pyrophosphorylase; GlgP, glycogen phosphorylase; GlgX, glycogen debranching enzyme; and GlgA, glycogen synthase) or chlamydial transporters (UhpC, G6P import protein). Previous trees often used automated phylogenomic pipelines that relied on single-matrix (usually best-fit) substitution models (e.g., LG, WAG) that could potentially provide incorrect inference due to rate heterogeneity across sites (Morgan et al., 2013). Based on their results, the authors (Domman et al., 2015) argued that GlgC and GlgP now show evidence of being of cyanobacterial and host origin, respectively, that Chlamydiales and Archaeplastida are united by the LGT (Lateral Gene Transfer) of GlgX but that the direction of transfer from chlamydiales to Archaeplastida is no longer clear. Furthermore, our hypothesis that chlamydiales have provided GlgA and UhpC to the Archaeplastida is now in question. Below, we inspect these issues in detail.
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Molecular evolution accompanying functional divergence of duplicated genes along the plant starch biosynthesis pathway
BMC evolutionary biology, 2014Co-Authors: Odrade Nougué, Steven G Ball, Jonathan Corbi, Domenica Manicacci, Maud I. TenaillonAbstract:Background Starch is the main source of carbon storage in the Archaeplastida. The starch biosynthesis pathway (sbp) emerged from cytosolic glycogen metabolism shortly after plastid endosymbiosis and was redirected to the plastid stroma during the green lineage divergence. The SBP is a complex network of genes, most of which are members of large multigene families. While some gene duplications occurred in the Archaeplastida ancestor, most were generated during the sbp redirection process, and the remaining few paralogs were generated through compartmentalization or tissue specialization during the evolution of the land plants. In the present study, we tested models of duplicated gene evolution in order to understand the evolutionary forces that have led to the development of SBP in angiosperms. We combined phylogenetic analyses and tests on the rates of evolution along branches emerging from major duplication events in six gene families encoding sbp enzymes.
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Chlamydia, cyanobiont, or host: who was on top in the ménage à trois?
Trends in Plant Science, 2013Co-Authors: Fabio Facchinelli, Christophe Colleoni, Steven G Ball, Andreas P. M. WeberAbstract:: The endosymbiont hypothesis proposes that photosynthate from the cyanobiont was exported to the cytosol of the eukaryote host and polymerized from ADP-glucose into glycogen. Chlamydia-like pathogens are the second major source of foreign genes in Archaeplastida, suggesting that these obligate intracellular pathogens had a significant role during the establishment of endosymbiosis, likely through facilitating the metabolic integration between the endosymbiont and the eukaryotic host. In this opinion article, we propose that a hexose phosphate transporter of chlamydial origin was the first transporter responsible for exporting photosynthate out of the cyanobiont. This connection pre-dates the recruitment of the host-derived carbon translocators on the plastid inner membranes of green and red algae, land plants, and photosynthetic organisms of higher order endosymbiotic origin.
Christophe Colleoni - One of the best experts on this subject based on the ideXlab platform.
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Host-pathogen biotic interactions shaped vitamin K metabolism in Archaeplastida
Scientific reports, 2018Co-Authors: Ugo Cenci, Christophe Colleoni, Derifa Kadouche, Hongyu Qiu, Trestan Pillonel, Pierre Cardol, Claire Remacle, Malika Chabi, Gilbert Greub, Debashish BhattacharyaAbstract:Menaquinone (vitamin K2) shuttles electrons between membrane-bound respiratory complexes under microaerophilic conditions. In photosynthetic eukaryotes and cyanobacteria, phylloquinone (vitamin K1) participates in photosystem I function. Here we elucidate the evolutionary history of vitamin K metabolism in algae and plants. We show that Chlamydiales intracellular pathogens made major genetic contributions to the synthesis of the naphthoyl ring core and the isoprenoid side-chain of these quinones. Production of the core in extremophilic red algae is under control of a menaquinone (Men) gene cluster consisting of 7 genes that putatively originated via lateral gene transfer (LGT) from a chlamydial donor to the plastid genome. In other green and red algae, functionally related nuclear genes also originated via LGT from a non-cyanobacterial, albeit unidentified source. In addition, we show that 3–4 of the 9 required steps for synthesis of the isoprenoid side chains are under control of genes of chlamydial origin. These results are discussed in the light of the hypoxic response experienced by the cyanobacterial endosymbiont when it gained access to the eukaryotic cytosol.
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Convergent Evolution of Starch Metabolism in Cyanobacteria and Archaeplastida
Evolutionary Biology, 2016Co-Authors: Christophe Colleoni, Ugo CenciAbstract:It is widely accepted that Archaeplastida phylum comprising Glaucophyta, Rhodophyta, and Chloroplastida originates from a unique endosymbiosis event, called primary plastid endosymbiosis, between a cyanobacterium and a eukaryotic cell. In addition to acquiring oxygenic photosynthesis, the three sister lineages gained the ability to synthesize a novel semi-crystalline storage polysaccharide: starch. In Archaeplastida, several lines of evidence reveal that the transition from glycogen synthesis to starch accumulation results in the recruitment of an isoamylase (ISA)-type debranching enzyme. The latter removes short-branched glucan chains, which prevent amylopectin crystallization. Recently, a small group of unicellular diazotrophic cyanobacteria, possibly the closest relative of the ancestral plastid, have been reported accumulating starch-like granules composed of both amylose and amylopectin fractions instead of glycogen particles. In order to understand starch metabolism in this particular group of cyanobacteria, a random mutagenesis was carried out on the unicellular starch-accumulating Cyanobacterium sp. CLg1. Throughout iodine crystal vapors screening, fourteen mutant strains have substituted starch granules by that of glycogen particles. Interestingly, such as in plants, all mutant strains were impaired in an isoamylase-type debranching enzyme activity. However, phylogenetic analyses point out that the critical step for starch crystallization in Archaeplastida did not evolve from the cyanobacterial isoamylase/glgX gene, but from another pathogenic bacteria. Based on this work, it appears that the transition from glycogen to starch has evolved independently in both cyanobacteria and Archaeplastida by following a common glucan trimming mechanism.
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was the chlamydial adaptative strategy to tryptophan starvation an early determinant of plastid endosymbiosis
Frontiers in Cellular and Infection Microbiology, 2016Co-Authors: Ugo Cenci, Christophe Colleoni, Mathieu Ducatez, Derifa Kadouche, Steven G BallAbstract:Chlamydiales were recently proposed to have sheltered the future cyanobacterial ancestor of plastids in a common inclusion. The intracellular pathogens are thought to have donated those critical transporters that triggered the efflux of photosynthetic carbon and the consequent onset of symbiosis. Chlamydiales are also suspected to have encoded glycogen metabolism TTS (Type Three Secretion) effectors responsible for photosynthetic carbon assimilation in the eukaryotic cytosol. We now review the reasons underlying other chlamydial lateral gene transfers (LGT) evidenced in the descendants of plastid endosymbiosis. In particular, we show that half of the genes encoding enzymes of tryptophan synthesis in Archaeplastida are of chlamydial origin. Tryptophan is known to define an essential cue triggering two alternative modes of replication in Chlamydiales. In addition, sophisticated tryptophan starvation mechanisms are known to have been implemented as antibacterial defenses by their eukaryotic hosts. We propose that Chlamydiales have donated their tryptophan operon to the emerging plastid to ensure increased synthesis of tryptophan by the plastid ancestor. This would have allowed massive expression of the tryptophan rich chlamydial transporters responsible for symbiosis. It would also have allowed possible export of this valuable amino-acid in the inclusion of the tryptophan hungry pathogens. Free-living single cell cyanobacteria are devoid of proteins able to transport this amino-acid. We therefore investigated the phylogeny of the E.coli Tyr/Trp transporters and found yet another LGT from Chlamydiales to Archaeplastida thereby considerably strengthening our proposal.
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Chlamydia, cyanobiont, or host: who was on top in the ménage à trois?
Trends in Plant Science, 2013Co-Authors: Fabio Facchinelli, Christophe Colleoni, Steven G Ball, Andreas P. M. WeberAbstract:: The endosymbiont hypothesis proposes that photosynthate from the cyanobiont was exported to the cytosol of the eukaryote host and polymerized from ADP-glucose into glycogen. Chlamydia-like pathogens are the second major source of foreign genes in Archaeplastida, suggesting that these obligate intracellular pathogens had a significant role during the establishment of endosymbiosis, likely through facilitating the metabolic integration between the endosymbiont and the eukaryotic host. In this opinion article, we propose that a hexose phosphate transporter of chlamydial origin was the first transporter responsible for exporting photosynthate out of the cyanobiont. This connection pre-dates the recruitment of the host-derived carbon translocators on the plastid inner membranes of green and red algae, land plants, and photosynthetic organisms of higher order endosymbiotic origin.
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Transition from glycogen to starch metabolism in Archaeplastida.
Trends in Plant Science, 2013Co-Authors: Ugo Cenci, Christophe Colleoni, Felix Nitschke, Martin Steup, Berge A Minassian, Steven G BallAbstract:: In this opinion article we propose a scenario detailing how two crucial components have evolved simultaneously to ensure the transition of glycogen to starch in the cytosol of the Archaeplastida last common ancestor: (i) the recruitment of an enzyme from intracellular Chlamydiae pathogens to facilitate crystallization of α-glucan chains; and (ii) the evolution of novel types of polysaccharide (de)phosphorylating enzymes from preexisting glycogen (de)phosphorylation host pathways to allow the turnover of such crystals. We speculate that the transition to starch benefitted Archaeplastida in three ways: more carbon could be packed into osmotically inert material; the host could resume control of carbon assimilation from the chlamydial pathogen that triggered plastid endosymbiosis; and cyanobacterial photosynthate export could be integrated in the emerging Archaeplastida.
Philippe Deschamps - One of the best experts on this subject based on the ideXlab platform.
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an early branching freshwater cyanobacterium at the origin of plastids
Current Biology, 2017Co-Authors: Rafael I Poncetoledo, Philippe Deschamps, Purificacion Lopezgarcia, Yvan Zivanovic, Karim Benzerara, David MoreiraAbstract:Summary Photosynthesis evolved in eukaryotes by the endosymbiosis of a cyanobacterium, the future plastid, within a heterotrophic host. This primary endosymbiosis occurred in the ancestor of Archaeplastida, a eukaryotic supergroup that includes glaucophytes, red algae, green algae, and land plants [1–4]. However, although the endosymbiotic origin of plastids from a single cyanobacterial ancestor is firmly established, the nature of that ancestor remains controversial: plastids have been proposed to derive from either early- or late-branching cyanobacterial lineages [5–11]. To solve this issue, we carried out phylogenomic and supernetwork analyses of the most comprehensive dataset analyzed so far including plastid-encoded proteins and nucleus-encoded proteins of plastid origin resulting from endosymbiotic gene transfer (EGT) of primary photosynthetic eukaryotes, as well as wide-ranging genome data from cyanobacteria, including novel lineages. Our analyses strongly support that plastids evolved from deep-branching cyanobacteria and that the present-day closest cultured relative of primary plastids is Gloeomargarita lithophora . This species belongs to a recently discovered cyanobacterial lineage widespread in freshwater microbialites and microbial mats [12, 13]. The ecological distribution of this lineage sheds new light on the environmental conditions where the emergence of photosynthetic eukaryotes occurred, most likely in a terrestrial-freshwater setting. The fact that glaucophytes, the first archaeplastid lineage to diverge, are exclusively found in freshwater ecosystems reinforces this hypothesis. Therefore, not only did plastids emerge early within cyanobacteria, but the first photosynthetic eukaryotes most likely evolved in terrestrial-freshwater settings, not in oceans as commonly thought.
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Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates?
Acta Societatis Botanicorum Poloniae, 2014Co-Authors: Philippe DeschampsAbstract:Eukaryotes acquired the ability to process photosynthesis by engulfing a cyanobacterium and transforming it into a genuine organelle called the plastid. This event, named primary endosymbiosis, occurred once more than a billion years ago, and allowed the emergence of the Archaeplastida, a monophyletic supergroup comprising the green algae and plants, the red algae and the glaucophytes. Of the other known cases of symbiosis between cyanobacteria and eukaryotes, none has achieved a comparable level of cell integration nor reached the same evolutionary and ecological success than primary endosymbiosis did. Reasons for this unique accomplishment are still unknown and difficult to comprehend. The exploration of plant genomes has revealed a considerable amount of genes closely related to homologs of Chlamydiae bacteria, and probably acquired by horizontal gene transfer. Several studies have proposed that these transferred genes, which are mostly involved in the functioning of the plastid, may have helped the settlement of primary endosymbiosis. Some of these studies propose that Chlamydiae and cyanobacterial symbionts coexisted in the eukaryotic host of the primary endosymbiosis, and that Chlamydiae provided solutions for the metabolic symbiosis between the cyanobacterium and the host, ensuring the success of primary endosymbiosis. In this review, I present a reevaluation of the contribution of Chlamydiae genes to the genome of Archaeplastida and discuss the strengths and weaknesses of this tripartite model for primary endosymbiosis.
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Genetic dissection of floridean starch synthesis in the cytosol of the model dinoflagellate Crypthecodinium cohnii.
Proceedings of the National Academy of Sciences of the United States of America, 2009Co-Authors: David Dauvillée, Philippe Deschamps, Jean-luc Putaux, Jean-philippe Ral, Charlotte Plancke, Jimi Devassine, Amandine Durand-terrasson, Aline Devin, Steven BallAbstract:Starch defines an insoluble semicrystalline form of storage polysaccharides restricted to Archaeplastida (red and green algae, land plants, and glaucophytes) and some secondary endosymbiosis derivatives of the latter. While green algae and land-plants store starch in plastids by using an ADP-glucose-based pathway related to that of cyanobacteria, red algae, glaucophytes, cryptophytes, dinoflagellates, and apicomplexa parasites store a similar type of polysaccharide named floridean starch in their cytosol or periplast. These organisms are suspected to store their floridean starch from UDP-glucose in a fashion similar to heterotrophic eukaryotes. However, experimental proof of this suspicion has never been produced. Dinoflagellates define an important group of both photoautotrophic and heterotrophic protists. We now report the selection and characterization of a low starch mutant of the heterotrophic dinoflagellate Crypthecodinium cohnii. We show that the sta1-1 mutation of C. cohnii leads to a modification of the UDP-glucose-specific soluble starch synthase activity that correlates with a decrease in starch content and an alteration of amylopectin structure. These experimental results validate the UDP-glucose-based pathway proposed for floridean starch synthesis.
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Signal Conflicts in the Phylogeny of the Primary Photosynthetic Eukaryotes
Molecular Biology and Evolution, 2009Co-Authors: Philippe Deschamps, David MoreiraAbstract:It is widely accepted that the first photosynthetic eukaryotes arose from a single primary endosymbiosis of a cyanobacterium in a phagotrophic eukaryotic host, which led to the emergence of three major lineages: Chloroplastida (green algae and land plants), Rhodophyta, and Glaucophyta. For a long time, Glaucophyta have been thought to represent the earliest branch among them. However, recent massive phylogenomic analyses of nuclear genes have challenged this view, because most of them suggested a basal position of Rhodophyta, though with moderate statistical support. We have addressed this question by phylogenomic analysis of a large data set of 124 proteins transferred from the chloroplast to the nuclear genome of the three Archaeplastida lineages. In contrast to previous analyses, we found strong support for the basal emergence of the Chloroplastida and the sister-group relationship of Glaucophyta and Rhodophyta. Moreover, the reanalysis of chloroplast gene sequences using methods more robust against compositional and evolutionary rate biases sustained the same result. Finally, we observed that the basal position of Rhodophyta found in the phylogenies based on nuclear genes depended on the sampling of sequences used as outgroup. When eukaryotes supposed to have never had plastids (animals and fungi) were used, the analysis strongly supported the early emergence of Glaucophyta instead of Rhodophyta. Therefore, there is a conflicting signal between genes of different evolutionary origins supporting either the basal branching of Glaucophyta or of Chloroplastida within the Archaeplastida. This second possibility would agree with the existence of the subkingdom Biliphyta, joining Glaucophyta and Rhodophyta.
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The relocation of starch metabolism to chloroplasts: when, why and how
Trends in Plant Science, 2008Co-Authors: Philippe Deschamps, Christophe D'hulst, H. Ekkehard Neuhaus, Ilka Haferkamp, Steven G BallAbstract:Plastid endosymbiosis was accompanied by the appearance of a novel type of semi-cristalline storage polysaccharide (starch). Interestingly, starch is found in the cytoplasm of Rhodophyceae and Glaucophyta but is localized to the chloroplast stroma of Chloroplastida. The pathway is presumed to have been cytosolic in the common ancestor of the three Archaeplastida lineages. The means by which in green plants and algae an entire suite of nuclear-encoded starch-metabolism genes could have had their protein products rewired simultaneously to plastids are unclear. This opinion article reviews the timing and the possible reasons underlying this rewiring and proposes a hypothesis that explains its mechanism. The consequences of this mechanism on the complexity of starch metabolism in Chloroplastida are discussed.
Andreas P. M. Weber - One of the best experts on this subject based on the ideXlab platform.
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Evolution of Photorespiratory Glycolate Oxidase among Archaeplastida
Plants (Basel Switzerland), 2020Co-Authors: Ramona Kern, Fabio Facchinelli, Andreas P. M. Weber, Charles F. Delwiche, Hermann Bauwe, Martin HagemannAbstract:Photorespiration has been shown to be essential for all oxygenic phototrophs in the present-day oxygen-containing atmosphere. The strong similarity of the photorespiratory cycle in cyanobacteria and plants led to the hypothesis that oxygenic photosynthesis and photorespiration co-evolved in cyanobacteria, and then entered the eukaryotic algal lineages up to land plants via endosymbiosis. However, the evolutionary origin of the photorespiratory enzyme glycolate oxidase (GOX) is controversial, which challenges the common origin hypothesis. Here, we tested this hypothesis using phylogenetic and biochemical approaches with broad taxon sampling. Phylogenetic analysis supported the view that a cyanobacterial GOX-like protein of the 2-hydroxy-acid oxidase family most likely served as an ancestor for GOX in all eukaryotes. Furthermore, our results strongly indicate that GOX was recruited to the photorespiratory metabolism at the origin of Archaeplastida, because we verified that Glaucophyta, Rhodophyta, and Streptophyta all express GOX enzymes with preference for the substrate glycolate. Moreover, an “ancestral” protein synthetically derived from the node separating all prokaryotic from eukaryotic GOX-like proteins also preferred glycolate over l-lactate. These results support the notion that a cyanobacterial ancestral protein laid the foundation for the evolution of photorespiratory GOX enzymes in modern eukaryotic phototrophs.
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Genomics-Informed Insights into Endosymbiotic Organelle Evolution in Photosynthetic Eukaryotes.
Annual review of plant biology, 2018Co-Authors: Eva C. M. Nowack, Andreas P. M. WeberAbstract:The conversion of free-living cyanobacteria to photosynthetic organelles of eukaryotic cells through endosymbiosis transformed the biosphere and eventually provided the basis for life on land. Despite the presumable advantage conferred by the acquisition of photoautotrophy through endosymbiosis, only two independent cases of primary endosymbiosis have been documented: one that gave rise to the Archaeplastida, and the other to photosynthetic species of the thecate, filose amoeba Paulinella. Here, we review recent genomics-informed insights into the primary endosymbiotic origins of cyanobacteria-derived organelles. Furthermore, we discuss the preconditions for the evolution of nitrogen-fixing organelles. Recent genomic data on previously undersampled cyanobacterial and protist taxa provide new clues to the origins of the host cell and endosymbiont, and proteomic approaches allow insights into the rearrangement of the endosymbiont proteome during organellogenesis. We conclude that in addition to endosymbioti...
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Commentary: Plastid establishment did not require a chlamydial partner.
Frontiers in cellular and infection microbiology, 2016Co-Authors: Steven G Ball, Debashish Bhattacharya, Huan Qiu, Andreas P. M. WeberAbstract:Several groups have independently proposed an active role for Chlamydiales in primary plastid establishment in Archaeplastida (Huang and Gogarten, 2007; Becker et al., 2008; Moustafa et al., 2008). We relied on a combination of biochemical and phylogenetic evidence to erect the MAT (Menage a Trois) hypothesis (Ball et al., 2013; Facchinelli et al., 2013). Under this scenario, Chlamydiales sheltered the once free-living cyanobacterial plastid ancestor from host defenses and provided critical components such as carbohydrate transporters and protein effectors that allowed the storage of exported carbohydrates into host glycogen pools. A recent paper by Domman et al. (2015) reassessed the phylogenies published by us and others on these components. These authors applied evolutionary models that better account for across-site and across-branch sequence compositional variation (i.e., Bayesian approaches with the CAT family of evolutionary models Lartillot and Philippe, 2004) to reanalyze proteins involved in glycogen metabolism. These are either chlamydial effectors (GlgC, ADP-glucose pyrophosphorylase; GlgP, glycogen phosphorylase; GlgX, glycogen debranching enzyme; and GlgA, glycogen synthase) or chlamydial transporters (UhpC, G6P import protein). Previous trees often used automated phylogenomic pipelines that relied on single-matrix (usually best-fit) substitution models (e.g., LG, WAG) that could potentially provide incorrect inference due to rate heterogeneity across sites (Morgan et al., 2013). Based on their results, the authors (Domman et al., 2015) argued that GlgC and GlgP now show evidence of being of cyanobacterial and host origin, respectively, that Chlamydiales and Archaeplastida are united by the LGT (Lateral Gene Transfer) of GlgX but that the direction of transfer from chlamydiales to Archaeplastida is no longer clear. Furthermore, our hypothesis that chlamydiales have provided GlgA and UhpC to the Archaeplastida is now in question. Below, we inspect these issues in detail.
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Metabolic connectivity as a driver of host and endosymbiont integration
Proceedings of the National Academy of Sciences of the United States of America, 2015Co-Authors: Slim Karkar, Dana C. Price, Fabio Facchinelli, Andreas P. M. Weber, Debashish BhattacharyaAbstract:The origin of oxygenic photosynthesis in the Archaeplastida common ancestor was foundational for the evolution of multicellular life. It is very likely that the primary endosymbiosis that explains plastid origin relied initially on the establishment of a metabolic connection between the host cell and captured cyanobacterium. We posit that these connections were derived primarily from existing host-derived components. To test this idea, we used phylogenomic and network analysis to infer the phylogenetic origin and evolutionary history of 37 validated plastid innermost membrane (permeome) metabolite transporters from the model plant Arabidopsis thaliana. Our results show that 57% of these transporter genes are of eukaryotic origin and that the captured cyanobacterium made a relatively minor (albeit important) contribution to the process. We also tested the hypothesis that the bacterium-derived hexose-phosphate transporter UhpC might have been the primordial sugar transporter in the Archaeplastida ancestor. Bioinformatic and protein localization studies demonstrate that this protein in the extremophilic red algae Galdieria sulphuraria and Cyanidioschyzon merolae are plastid targeted. Given this protein is also localized in plastids in the glaucophyte alga Cyanophora paradoxa, we suggest it played a crucial role in early plastid endosymbiosis by connecting the endosymbiont and host carbon storage networks. In summary, our work significantly advances understanding of plastid integration and favors a host-centric view of endosymbiosis. Under this view, nuclear genes of either eukaryotic or bacterial (noncyanobacterial) origin provided key elements of the toolkit needed for establishing metabolic connections in the primordial Archaeplastida lineage.
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Assessing the bacterial contribution to the plastid proteome
Trends in plant science, 2013Co-Authors: Huan Qiu, Dana C. Price, Fabio Facchinelli, Hwan Su Yoon, Andreas P. M. Weber, Debashish BhattacharyaAbstract:Plastids fulfill a variety of different functions (e.g., photosynthesis and amino acid biosynthesis) that rely on proteins of cyanobacterial (i.e., endosymbiont), noncyanobacterial, and ‘host’ (eukaryotic) origins. Analysis of plastid proteome data from glaucophytes and green algae allows robust inference of protein origins and organelle protein sharing across the >1 billion years of Archaeplastida evolution. Here, we show that more than one-third of genes encoding plastid proteins lack detectable homologs in Cyanobacteria, underlining the taxonomically broad contributions to plastid functions. Chlamydiae and Proteobacteria are the most significant other bacterial sources of plastid proteins. Mapping of plastid proteins to metabolic pathways shows a core set of anciently derived proteins in Archaeplastida, with many others being lineage specific and derived from independent horizontal gene transfer (HGT) events.
