RESUMEN
Cryptophyte and chlorarachniophyte algae are transitional forms in the widespread secondary endosymbiotic acquisition of photosynthesis by engulfment of eukaryotic algae. Unlike most secondary plastid-bearing algae, miniaturized versions of the endosymbiont nuclei (nucleomorphs) persist in cryptophytes and chlorarachniophytes. To determine why, and to address other fundamental questions about eukaryote-eukaryote endosymbiosis, we sequenced the nuclear genomes of the cryptophyte Guillardia theta and the chlorarachniophyte Bigelowiella natans. Both genomes have >21,000 protein genes and are intron rich, and B. natans exhibits unprecedented alternative splicing for a single-celled organism. Phylogenomic analyses and subcellular targeting predictions reveal extensive genetic and biochemical mosaicism, with both host- and endosymbiont-derived genes servicing the mitochondrion, the host cell cytosol, the plastid and the remnant endosymbiont cytosol of both algae. Mitochondrion-to-nucleus gene transfer still occurs in both organisms but plastid-to-nucleus and nucleomorph-to-nucleus transfers do not, which explains why a small residue of essential genes remains locked in each nucleomorph.
Asunto(s)
Núcleo Celular/genética , Cercozoos/genética , Criptófitas/genética , Evolución Molecular , Genoma/genética , Mosaicismo , Simbiosis/genética , Proteínas Algáceas/genética , Proteínas Algáceas/metabolismo , Empalme Alternativo/genética , Cercozoos/citología , Cercozoos/metabolismo , Criptófitas/citología , Criptófitas/metabolismo , Citosol/metabolismo , Duplicación de Gen/genética , Transferencia de Gen Horizontal/genética , Genes Esenciales/genética , Genoma Mitocondrial/genética , Genoma de Planta/genética , Genoma de Plastidios/genética , Datos de Secuencia Molecular , Filogenia , Transporte de Proteínas , Proteoma/genética , Proteoma/metabolismo , Transcriptoma/genéticaRESUMEN
Eukaryotes acquired photosynthetic metabolism over a billion years ago, and during that time the light-harvesting antennae have undergone significant structural and functional divergence. The antenna systems are generally used to harvest and transfer excitation energy into the reaction centers to drive photosynthesis, but also have the dual role of energy dissipation. Phycobilisomes formed the first antenna system in oxygenic photoautotrophs, and this soluble protein complex continues to be the dominant antenna in extant cyanobacteria, glaucophytes, and red algae. However, phycobilisomes were lost multiple times during eukaryotic evolution in favor of a thylakoid membrane-integral light-harvesting complex (LHC) antenna system found in the majority of eukaryotic taxa. While photosynthesis spread across different eukaryotic kingdoms via endosymbiosis, the antenna systems underwent extensive modification as photosynthetic groups optimized their light-harvesting capacity and ability to acclimate to changing environmental conditions. This review discusses the different classes of LHCs within photosynthetic eukaryotes and examines LHC diversification in different groups in a structural and functional context.
Asunto(s)
Eucariontes/metabolismo , Complejos de Proteína Captadores de Luz/metabolismo , Fotosíntesis , Clorofila/metabolismo , Evolución Molecular , Complejos de Proteína Captadores de Luz/genética , FilogeniaRESUMEN
Light-harvesting-like (LIL) proteins are low-molecular-mass membrane proteins related to the light-harvesting complexes, which form the dominant antenna system in most photosynthetic eukaryotes. To analyze the LIL protein family, we mined a number of publicly available databases to identify members of this family in a broad range of organisms. LIL proteins are diverse, having one to three predicted transmembrane helices. One- and two-helix LIL proteins were found in all the major photosynthetic eukaryote lineages (glaucophytes, red algae, and green algae) and are particularly well conserved in the green algae and land plants. In most cases, however, these proteins are not conserved between major lineages, and in some cases appear to have evolved independently. Three-helix LIL proteins are well conserved within the gymnosperms and angiosperms, but are much more divergent, and have been duplicated multiple times, in the green algae and bryophytes. We also identified a novel LIL protein in two Micromonas strains that contains a fourth hydrophobic region. This analysis identifies conserved members of the LIL protein family, signifying their importance to photosynthetic eukaryotes. It also indicates that classification of these proteins based on structural characteristics alone inadequately reflects the evolutionary history observed in this complex protein family.
Asunto(s)
Eucariontes/genética , Evolución Molecular , Complejos de Proteína Captadores de Luz/genética , Fotosíntesis/genética , Clorofila/metabolismo , Criptófitas/genética , Criptófitas/metabolismo , Eucariontes/metabolismo , Genoma , Complejos de Proteína Captadores de Luz/química , Fotosíntesis/fisiología , Unión Proteica , Dominios y Motivos de Interacción de Proteínas/genética , Estructura Secundaria de Proteína/genéticaRESUMEN
Chlorarachniophytes are unicellular marine algae with plastids (chloroplasts) of secondary endosymbiotic origin. Chlorarachniophyte cells retain the remnant nucleus (nucleomorph) and cytoplasm (periplastidial compartment, PPC) of the green algal endosymbiont from which their plastid was derived. To characterize the diversity of nucleus-encoded proteins targeted to the chlorarachniophyte plastid, nucleomorph, and PPC, we isolated plastid-nucleomorph complexes from the model chlorarachniophyte Bigelowiella natans and subjected them to high-pressure liquid chromatography-tandem mass spectrometry. Our proteomic analysis, the first of its kind for a nucleomorph-bearing alga, resulted in the identification of 324 proteins with 95% confidence. Approximately 50% of these proteins have predicted bipartite leader sequences at their amino termini. Nucleus-encoded proteins make up >90% of the proteins identified. With respect to biological function, plastid-localized light-harvesting proteins were well represented, as were proteins involved in chlorophyll biosynthesis. Phylogenetic analyses revealed that many, but by no means all, of the proteins identified in our proteomic screen are of apparent green algal ancestry, consistent with the inferred evolutionary origin of the plastid and nucleomorph in chlorarachniophytes.
Asunto(s)
Proteínas Algáceas/metabolismo , Cercozoos/química , Proteoma/química , Proteínas Algáceas/química , Núcleo Celular/metabolismo , Cercozoos/metabolismo , Clorofila/biosíntesis , Cloroplastos/metabolismo , Fotosíntesis , Filogenia , Señales de Clasificación de Proteína , Transporte de Proteínas , Proteoma/metabolismo , ProteómicaRESUMEN
The primary endosymbiotic origin of the plastid in eukaryotes more than 1 billion years ago led to the evolution of algae and plants. We analyzed draft genome and transcriptome data from the basally diverging alga Cyanophora paradoxa and provide evidence for a single origin of the primary plastid in the eukaryote supergroup Plantae. C. paradoxa retains ancestral features of starch biosynthesis, fermentation, and plastid protein translocation common to plants and algae but lacks typical eukaryotic light-harvesting complex proteins. Traces of an ancient link to parasites such as Chlamydiae were found in the genomes of C. paradoxa and other Plantae. Apparently, Chlamydia-like bacteria donated genes that allow export of photosynthate from the plastid and its polymerization into storage polysaccharide in the cytosol.