Plastid evolution Gould, Sven B; Waller, Ross F; McFadden, Geoffrey I
Annual review of plant biology,
01/2008, Volume:
59
Journal Article
Peer reviewed
The ancestors of modern cyanobacteria invented O(2)-generating photosynthesis some 3.6 billion years ago. The conversion of water and CO(2) into energy-rich sugars and O(2) slowly transformed the ...planet, eventually creating the biosphere as we know it today. Eukaryotes didn't invent photosynthesis; they co-opted it from prokaryotes by engulfing and stably integrating a photoautotrophic prokaryote in a process known as primary endosymbiosis. After approximately a billion of years of coevolution, the eukaryotic host and its endosymbiont have achieved an extraordinary level of integration and have spawned a bewildering array of primary producers that now underpin life on land and in the water. No partnership has been more important to life on earth. Secondary endosymbioses have created additional autotrophic eukaryotic lineages that include key organisms in the marine environment. Some of these organisms have subsequently reverted to heterotrophic lifestyles, becoming significant pathogens, microscopic predators, and consumers. We review the origins, integration, and functions of the different plastid types with special emphasis on their biochemical abilities, transfer of genes to the host, and the back supply of proteins to the endosymbiont.
Dinoflagellates are key species in marine environments, but they remain poorly understood in part because of their large, complex genomes, unique molecular biology, and unresolved in-group ...relationships. We created a taxonomically representative dataset of dinoflagellate transcriptomes and used this to infer a strongly supported phylogeny to map major morphological and molecular transitions in dinoflagellate evolution. Our results show an earlybranching position of Noctiluca, monophyly of thecate (plate-bearing) dinoflagellates, and paraphyly of athecate ones. This represents unambiguous phylogenetic evidence for a single origin of the group’s cellulosic theca, which we show coincided with a radiation of cellulases implicated in cell division. By integrating dinoflagellate molecular, fossil, and biogeochemical evidence, we propose a revised model for the evolution of thecal tabulations and suggest that the late acquisition of dinosterol in the group is inconsistent with dinoflagellates being the source of this biomarker in pre-Mesozoic strata. Three distantly related, fundamentally nonphotosynthetic dinoflagellates, Noctiluca, Oxyrrhis, and Dinophysis, contain cryptic plastidial metabolisms and lack alternative cytosolic pathways, suggesting that all free-living dinoflagellates are metabolically dependent on plastids. This finding led us to propose general mechanisms of dependency on plastid organelles in eukaryotes that have lost photosynthesis; it also suggests that the evolutionary origin of bioluminescence in nonphotosynthetic dinoflagellates may be linked to plastidic tetrapyrrole biosynthesis. Finally, we use our phylogenetic framework to show that dinoflagellate nuclei have recruited DNA-binding proteins in three distinct evolutionary waves, which included two independent acquisitions of bacterial histone-like proteins.
The packaging, expression, and maintenance of nuclear genomes using histone proteins is a ubiquitous and fundamental feature of eukaryotic cells, yet the phylum Dinoflagellata has apparently ...abandoned this model of nuclear organization. Their nuclei contain permanently condensed, liquid crystalline chromosomes that seemingly lack histone proteins, and contain remarkably large genomes. The molecular basis for this reorganization is poorly understood, as is the sequence of evolutionary events that led to such radical change. We have investigated nuclear organization in the closest relative to dinoflagellates, Perkinsus marinus, and an early-branching dinoflagellate, Hematodinium sp., to identify early changes that occurred during dinoflagellate nuclear evolution.
We show that P. marinus has a typical nuclear organization that is based on the four core histones. By the early divergence of Hematodinium sp., however, dinoflagellate genome size is dramatically enlarged, chromosomes are permanently condensed, and histones are scarcely detectable. In place of histones, we identify a novel, dominant family of nuclear proteins that is only found in dinoflagellates and, surprisingly, in a family of large algal viruses, the Phycodnaviridae. These new proteins, which we call DVNPs (dinoflagellate/viral nucleoproteins), are highly basic, bind DNA with similar affinity to histones, and occur in multiple posttranslationally modified forms. We find these proteins throughout all dinoflagellates, including early- and late-branching taxa, but not in P. marinus.
Gain of a major novel family of nucleoproteins, apparently from an algal virus, occurred early in dinoflagellate evolution and coincides with rapid and dramatic reorganization of the dinoflagellate nucleus.
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► Novel dominant DNA-binding protein DVNP was gained early in dinoflagellate evolution ► DVNP was likely gained by a lateral gene transfer from an algal virus ► Dinoflagellates containing DVNP have lost nucleosomal bulk packing of their DNA ► Histone proteins are highly divergent and very lowly expressed in dinoflagellates
The apical complex is the instrument of invasion used by apicomplexan parasites, and the conoid is a conspicuous feature of this apparatus found throughout this phylum. The conoid, however, is ...believed to be heavily reduced or missing from Plasmodium species and other members of the class Aconoidasida. Relatively few conoid proteins have previously been identified, making it difficult to address how conserved this feature is throughout the phylum, and whether it is genuinely missing from some major groups. Moreover, parasites such as Plasmodium species cycle through 3 invasive forms, and there is the possibility of differential presence of the conoid between these stages. We have applied spatial proteomics and high-resolution microscopy to develop a more complete molecular inventory and understanding of the organisation of conoid-associated proteins in the model apicomplexan Toxoplasma gondii. These data revealed molecular conservation of all conoid substructures throughout Apicomplexa, including Plasmodium, and even in allied Myzozoa such as Chromera and dinoflagellates. We reporter-tagged and observed the expression and location of several conoid complex proteins in the malaria model P. berghei and revealed equivalent structures in all of its zoite forms, as well as evidence of molecular differentiation between blood-stage merozoites and the ookinetes and sporozoites of the mosquito vector. Collectively, we show that the conoid is a conserved apicomplexan element at the heart of the invasion mechanisms of these highly successful and often devastating parasites.
Apicomplexan parasites cause major human disease and food insecurity. They owe their considerable success to highly specialized cell compartments and structures. These adaptations drive their ...recognition, nondestructive penetration, and elaborate reengineering of the host’s cells to promote their growth, dissemination, and the countering of host defenses. The evolution of unique apicomplexan cellular compartments is concomitant with vast proteomic novelty. Consequently, half of apicomplexan proteins are unique and uncharacterized. Here, we determine the steady-state subcellular location of thousands of proteins simultaneously within the globally prevalent apicomplexan parasite Toxoplasma gondii. This provides unprecedented comprehensive molecular definition of these unicellular eukaryotes and their specialized compartments, and these data reveal the spatial organizations of protein expression and function, adaptation to hosts, and the underlying evolutionary trajectories of these pathogens.
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•Using hyperLOPIT, Toxoplasma proteins were assigned to their cell location•Complex proteomes associated with host interaction and adaptation are identified•The atlas reveals sites and chronology of cell evolution of apicomplexan parasitism•Cell spatial organization corelates with regulatory and biochemical programs
Apicomplexan proteomes are substantially specific to these parasites, and many cellular compartments are highly specialized. Using spatial proteomic methods, Barylyuk et al. simultaneously map the locations of thousands of Toxoplasma proteins, resolving the genomic complexity of this pathogen within the context of its cell organelles, compartments, and structures.
The phylum Apicomplexa has been defined by the presence of the apical complex, a structure composed of secretory organelles and specific cytoskeletal elements. A conspicuous feature of the apical ...complex in many apicomplexans is the conoid, a hollow tapered barrel structure composed of tubulin fibers. In Toxoplasma gondii, the apical complex is a central site of convergence for calcium-related and lipid-mediated signaling pathways that coordinate conoid protrusion, microneme secretion, and actin polymerization, to initiate gliding motility. Through cutting-edge technologies, great progress has recently been made in discovering the structural subcomponents and proteins implicated in the biogenesis and stability of the apical complex and, in turn, these discoveries have shed new light on the function and evolution of this definitive structure.
Recent methods, such as proximity labeling, localization of organelle proteins by isotope tagging, and ultrastructure expansion microscopy, have greatly advanced the proteomic characterization of the different apical complex subcompartments.The subpellicular microtubules (SPMTs) are decorated by unique microtubule-associated proteins and emerge from the apical polar ring (APR) by an unknown mechanism. The conoid is composed of open tubulin fibers that are bent by the recently characterized DCX protein.Recently characterized proteins, such as AC9, AC10, and ERK7, are essential for the stability of the APR, the conoid, and the SPMTs.In addition to its structural complexity, the apical complex acts as a signaling hub by being the point of convergence for many regulatory pathways.Broad evidence suggests that the conoid is derived from the flagellar root apparatus.
African trypanosomes are dixenous eukaryotic parasites that impose a significant human and veterinary disease burden on sub-Saharan Africa. Diversity between species and life-cycle stages is ...concomitant with distinct host and tissue tropisms within this group. Here, the spatial proteomes of two African trypanosome species, Trypanosoma brucei and Trypanosoma congolense, are mapped across two life-stages. The four resulting datasets provide evidence of expression of approximately 5500 proteins per cell-type. Over 2500 proteins per cell-type are classified to specific subcellular compartments, providing four comprehensive spatial proteomes. Comparative analysis reveals key routes of parasitic adaptation to different biological niches and provides insight into the molecular basis for diversity within and between these pathogen species.
The apical complex is the definitive cell structure of phylum Apicomplexa, and is the focus of the events of host cell penetration and the establishment of intracellular parasitism. Despite the ...importance of this structure, its molecular composition is relatively poorly known and few studies have experimentally tested its functions. We have characterized a novel Toxoplasma gondii protein, RNG2, that is located at the apical polar ring--the common structural element of apical complexes. During cell division, RNG2 is first recruited to centrosomes immediately after their duplication, confirming that assembly of the new apical complex commences as one of the earliest events of cell replication. RNG2 subsequently forms a ring, with the carboxy- and amino-termini anchored to the apical polar ring and mobile conoid, respectively, linking these two structures. Super-resolution microscopy resolves these two termini, and reveals that RNG2 orientation flips during invasion when the conoid is extruded. Inducible knockdown of RNG2 strongly inhibits host cell invasion. Consistent with this, secretion of micronemes is prevented in the absence of RNG2. This block, however, can be fully or partially overcome by exogenous stimulation of calcium or cGMP signaling pathways, respectively, implicating the apical complex directly in these signaling events. RNG2 demonstrates for the first time a role for the apical complex in controlling secretion of invasion factors in this important group of parasites.
The nature of energy metabolism in apicomplexan parasites has been closely investigated in the recent years. Studies in Plasmodium spp. and Toxoplasma gondii in particular have revealed that these ...parasites are able to employ enzymes in non-traditional ways, while utilizing multiple anaplerotic routes into a canonical tricarboxylic acid (TCA) cycle to satisfy their energy requirements. Importantly, some life stages of these parasites previously considered to be metabolically quiescent are, in fact, active and able to adapt their carbon source utilization to survive. We compare energy metabolism across the life cycle of malaria parasites and consider how this varies in other apicomplexans and related organisms, while discussing how this can be exploited for therapeutic intervention in these diseases.
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