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Debashish Bhattacharya – One of the best experts on this subject based on the ideXlab platform.

  • The Algal Tree of Life from a Genomics Perspective
    Photosynthesis in Algae: Biochemical and Physiological Mechanisms, 2020
    Co-Authors: Debashish Bhattacharya, Dana C. Price

    Abstract:

    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, 2020
    Co-Authors: Arwa Gabr, Arthur R. Grossman, Debashish Bhattacharya

    Abstract:

    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, 2019
    Co-Authors: Camilla Ferrari, Debashish Bhattacharya, Dana C. Price, Sebastian Proost, Marcin Janowski, Zoran Nikoloski, Takayuki Tohge, Arren Bar-even, Jörg D. Becker, Alisdair Fernie

    Abstract:

    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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Steven G Ball – One of the best experts on this subject based on the ideXlab platform.

  • Analysis of an improved Cyanophora paradoxa genome assembly.
    DNA Research, 2019
    Co-Authors: Dana C. Price, Ursula Goodenough, Robyn Roth, Thamali Kariyawasam, Marek Mutwil, Camilla Ferrari, Fabio Facchinelli, Steven G Ball, Ugo Cenci

    Abstract:

    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, 2016
    Co-Authors: Ugo Cenci, Christophe Colleoni, Mathieu Ducatez, Derifa Kadouche, Steven G Ball

    Abstract:

    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, 2016
    Co-Authors: Steven G Ball, Debashish Bhattacharya, Huan Qiu, Andreas P. M. Weber

    Abstract:

    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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Christophe Colleoni – One of the best experts on this subject based on the ideXlab platform.

  • Host-pathogen biotic interactions shaped vitamin K metabolism in Archaeplastida
    Scientific reports, 2018
    Co-Authors: Ugo Cenci, Christophe Colleoni, Derifa Kadouche, Hongyu Qiu, Trestan Pillonel, Pierre Cardol, Claire Remacle, Malika Chabi, Gilbert Greub, Debashish Bhattacharya

    Abstract:

    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, 2016
    Co-Authors: Christophe Colleoni, Ugo Cenci

    Abstract:

    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, 2016
    Co-Authors: Ugo Cenci, Christophe Colleoni, Mathieu Ducatez, Derifa Kadouche, Steven G Ball

    Abstract:

    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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