Symbiotic Origin of a Novel Actin Gene in the Cryptophyte, Pyrenomonas Helgolandii (original) (raw)

Migration of the Plastid Genome to the Nucleus in a Peridinin Dinoflagellate

Current Biology, 2004

Our tally of photosynthetic genes is, however, likely to be an underestimate of the true number in the A. tamarense EST data set because we sequenced clones from the 3Ј terminus to maximize clustering accuracy by using Physiology, and Biophysics 4 Department of Electrical and the 3Ј untranslated region (UTR). Many of our cDNAs do not extend to the 5Ј portion of the transcript and Computer Engineering 5 Department of Ophthalmology and therefore lack information about the 5Ј plastid-targeting signal (potentially a useful tool for identifying plastid-Center for Bioinformatics and Computational Biology targeted proteins [see below]). Consequently, we were unable to distinguish between mitochondrial and cyto-The University of Iowa Iowa City, Iowa 52242 plasmic homologs of proteins that are also targeted to the plastid. Because of this limitation, we focused our analyses on proteins that are found on other plastid genomes or plastid-targeted proteins that could be un-Summary ambiguously distinguished from other cellular homologs through sequence similarity or phylogenetic analyses Dinoflagellate algae are important primary producers (e.g., hemB). We searched with the genes listed in Table and of significant ecological and economic impact be-

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

2012

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.

The Origin and Establishment of the Plastid in Algae and Plants

Annual Review of Genetics, 2007

The establishment of the photosynthetic organelle (plastid) in eukaryotes and the diversification of algae and plants were landmark evolutionary events because these taxa form the base of the food chain for many ecosystems on our planet. The plastid originated via a putative single, ancient primary endosymbiosis in which a heterotrophic protist engulfed and retained a cyanobacterium in its cytoplasm. Once successfully established, this plastid spread into other protist lineages through eukaryote-eukaryote (secondary and tertiary) endosymbioses. This process of serial cell capture and enslavement explains the diversity of photosynthetic eukaryotes. Recent genomic and phylogenomic approaches have significantly clarified plastid genome evolution, the movement of endosymbiont genes to the "host" nuclear genome (endosymbiotic gene transfer), and plastid spread throughout the eukaryotic tree of life. Here we review these aspects of plastid evolution with a focus on understanding early events in plastid endosymbiosis.

Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata

BMC genomics, 2010

Background: Dinophysis is exceptional among dinoflagellates, possessing plastids derived from cryptophyte algae. Although Dinophysis can be maintained in pure culture for several months, the genus is mixotrophic and needs to feed either to acquire plastids (a process known as kleptoplastidy) or obtain growth factors necessary for plastid maintenance. Dinophysis does not feed directly on cryptophyte algae, but rather on a ciliate (Myrionecta rubra) that has consumed the cryptophytes and retained their plastids. Despite the apparent absence of cryptophyte nuclear genes required for plastid function, Dinophysis can retain cryptophyte plastids for months without feeding.

Proteomics Reveals Plastid- and Periplastid-Targeted Proteins in the Chlorarachniophyte Alga Bigelowiella natans

Genome Biology and Evolution, 2012

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.

A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum

BMC Evolutionary Biology, 2010

Background: Plastid replacements through secondary endosymbioses include massive transfer of genes from the endosymbiont to the host nucleus and require a new targeting system to enable transport of the plastid-targeted proteins across 3-4 plastid membranes. The dinoflagellates are the only eukaryotic lineage that has been shown to have undergone several plastid replacement events, and this group is thus highly relevant for studying the processes involved in plastid evolution. In this study, we analyzed the phylogenetic origin and N-terminal extensions of plastid-targeted proteins from Lepidodinium chlorophorum, a member of the only dinoflagellate genus that harbors a green secondary plastid rather than the red algal-derived, peridinin-containing plastid usually found in photosynthetic dinoflagellates.

From cyanobacteria to plants: conservation of PII functions during plastid evolution

Planta, 2013

This article reviews the current state-of-the-art concerning the functions of the signal processing protein PII in cyanobacteria and plants, with a special focus on evolutionary aspects. We start out with a general introduction to PII proteins, their distribution, and their evolution. We also discuss PII-like proteins and domains, in particular, the similarity between ATP-phosphoribosyltransferase (ATP-PRT) and its PII-like domain and the complex between N-acetyl-L-glutamate kinase (NAGK) and its PII activator protein from oxygenic phototrophs. The structural basis of the function of PII as an ATP/ADP/ 2-oxoglutarate signal processor is described for Synechococcus elongatus PII. In both cyanobacteria and plants, a major target of PII regulation is NAGK, which catalyzes the committed step of arginine biosynthesis. The common principles of NAGK regulation by PII are outlined. Based on the observation that PII proteins from cyanobacteria and plants can functionally replace each other, the hypothesis that PII-dependent NAGK control was under selective pressure during the evolution of plastids of Chloroplastida and Rhodophyta is tested by bioinformatics approaches. It is noteworthy that two lineages of heterokont algae, diatoms and brown algae, also possess NAGK, albeit lacking PII; their NAGK however appears to have descended from an alphaproteobacterium and not from a cyanobacterium as in plants. We end this article by coming to the conclusion that during the evolution of plastids, PII lost its function in coordinating gene expression through the PipX-NtcA network but preserved its role in nitrogen (arginine) storage metabolism, and subsequently took over the fine-tuned regulation of carbon (fatty acid) storage metabolism, which is important in certain developmental stages of plants.

Hypothesis: Gene-rich plastid genomes in red algae may be an outcome of nuclear genome reduction

Journal of phycology, 2017

Red algae (Rhodophyta) putatively diverged from the eukaryote tree of life >1.2 billion years ago and are the source of plastids in the ecologically important diatoms, haptophytes, and dinoflagellates. In general, red algae contain the largest plastid gene inventory among all such organelles derived from primary, secondary, or additional rounds of endosymbiosis. In contrast, their nuclear gene inventory is reduced when compared to their putative sister lineage, the Viridiplantae, and other photosynthetic lineages. The latter is thought to have resulted from a phase of genome reduction that occurred in the stem lineage of Rhodophyta. A recent comparative analysis of a taxonomically broad collection of red algal and Viridiplantae plastid genomes demonstrates that the red algal ancestor encoded ~1.5× more plastid genes than Viridiplantae. This difference is primarily explained by more extensive endosymbiotic gene transfer (EGT) in the stem lineage of Viridiplantae, when compared to ...