Jeferson Gross

Cyanophora paradoxa Genome Elucidates Origin of Photosynthesis in Algae and Plants

Plastid Origins The glaucophytes, represented by the alga Cyanophora paradoxa, are the putative sister group of red and green algae and plants, which together comprise the founding group of photosynthetic eukaryotes, the Plantae. In their analysis of the genome of C. paradoxa, Price et al. (p. 843; see the Perspective by Spiegel) demonstrate a unique origin for the plastid in the ancestor of this supergroup, which retains much of the ancestral diversity in genes involved in carbohydrate metabolism and fermentation, as well as in the gene content of the mitochondrial genome. Moreover, about 3.3% of nuclear genes in C. paradoxa seem to carry a signal of cyanobacterial ancestry, and key genes involved in starch biosynthesis are derived from energy parasites such as Chlamydiae. Rapid radiation, reticulate evolution via horizontal gene transfer, high rates of gene divergence, loss, and replacement, may have diffused the evolutionary signals within this supergroup, which perhaps explains previous difficulties in resolving its evolutionary history. An ancient algal genome suggests a unique origin of the plastid in the ancestor to plants, algae, and glaucophytes. 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.

Mitochondrial and plastid evolution in eukaryotes: an outsiders' perspective

The eukaryotic organelles mitochondrion and plastid originated from eubacterial endosymbionts. Here we propose that, in both cases, prokaryote-to-organelle conversion was driven by the internalization of host-encoded factors progressing from the outer membrane of the endosymbionts towards the intermembrane space, inner membrane and finally the organelle interior. This was made possible by an outside-to-inside establishment in the endosymbionts of host-controlled protein-sorting components, which enabled the gradual integration of organelle functions into the nuclear genome. Such a convergent trajectory for mitochondrion and plastid establishment suggests a novel paradigm for organelle evolution that affects theories of eukaryogenesis.

Revaluating the evolution of the Toc and Tic protein translocons

The origin of the plastid from a cyanobacterial endosymbiont necessitated the establishment of specialized molecular machines (translocons) to facilitate the import of nuclear-encoded proteins into the organelle. To improve our understanding of the evolution of the translocons at the outer and inner envelope membrane of chloroplasts (Toc and Tic, respectively), we critically reassess the prevalent notion that their subunits have a function exclusive to protein import. We propose that many translocon components are multifunctional, conserving ancestral pre-endosymbiotic properties that predate their recruitment into the primitive translocon (putatively composed of subunits Toc34, Toc75 and Tic110 and associated chaperones). Multifunctionality seems to be a hallmark of the Tic complex, in which protein import is integrated with a broad array of plastid processes.

Plastid Origin and Evolution: New Models Provide Insights into Old Problems

Algae are defined by their photosynthetic organelles (plastids) that have had multiple independent origins in different phyla. These instances of organelle transfer significantly complicate inference of the tree of life for eukaryotes because the intracellular gene transfer (endosymbiotic gene transfer [EGT]) associated with each round of endosymbiosis generates highly chimeric algal nuclear genomes. In this Update we review the current state in the field of endosymbiosis research with a focus on the use of the photosynthetic amoeba Paulinella to advance our knowledge of plastid evolution and current ideas about the origin of the plastid translocons. These research areas have been revolutionized by the advent of modern genomic approaches.

Evolution of salt tolerance in a laboratory reared population of Chlamydomonas reinhardtii

Understanding the genetic underpinnings of adaptive traits in microalgae is important for the study of evolution and for applied uses. We used long-term selection under a regime of serial transfers with haploid populations of the green alga Chlamydomonas reinhardtii raised in liquid TAP medium containing 200 mM NaCl. After 1255 generations, evolved salt (ES) populations could grow as rapidly in high salt medium as progenitor cells (progenitor light [PL]). Transcriptome data were analysed to elucidate the basis of salt tolerance in ES cells when compared with PL cells and to cells incubated for 48 h in high salt medium (progenitor salt [PS], the short-term acclimation response). These data demonstrate that evolved and short-term acclimation responses to salt stress differ fundamentally from each other. Progenitor salt cells exhibit well-known responses to salt stress such as reduction in photosynthesis, upregulation of glycerophospholipid signaling, and upregulation of the transcription and translation machinery. In contrast, ES cells show downregulation of genes involved in the stress response and in transcription/translation. Our results suggest that gene-rich mixotrophic lineages such as C. reinhardtii may be able to adapt rapidly to abiotic stress engendered either by a rapidly changing climate or physical vicariance events that isolate populations in stressful environments.

Porphyra: Complex Life Histories in a Harsh Environment: P. umbilicalis, an Intertidal Red Alga for Genomic Analysis

Porphyra encompasses a large group of multicellular red algae that have a prominent gametophytic phase. The complex, heteromorphic life history of species in this genus, their remarkable resilience to high light and desiccation, ancient fossil records, and value as human food (e.g., laver, nori), make Porphyra a compelling model for genome sequencing. Sequencing of the nuclear genome of Porphyra umbilicalis from the northwestern Atlantic is currently in process. The ∼270 Mb genome of this alga is much larger than that of the unicellular acidophilic Cyanidioschyzon merolae (16.5 Mb), the only rhodophyte for which there is a fully sequenced genome, and is approximately twice as large as the Arabidopsis genome. Future analyses of the P. umbilicalis genome should provide opportunities for researchers to (1) develop an increased understanding of the ways in which these algae have adapted to severe physiological stresses, (2) elucidate the molecular features of development through the complex life history, and (3) define key components required for the transition of growth from a single cell to a multicellular organism.

Using Natural Selection to Explore the Adaptive Potential of Chlamydomonas reinhardtii

Improving feedstock is critical to facilitate the commercial utilization of algae, in particular in open pond systems where, due to the presence of competitors and pests, high algal growth rates and stress tolerance are beneficial. Here we raised laboratory cultures of the model alga Chlamydomonas reinhardtii under serial dilution to explore the potential of crop improvement using natural selection. The alga was evolved for 1,880 generations in liquid medium under continuous light (EL population). At the end of the experiment, EL cells had a growth rate that was 35% greater than the progenitor population (PL). The removal of acetate from the medium demonstrated that EL growth enhancement largely relied on efficient usage of this organic carbon source. Genome re-sequencing uncovered 1,937 polymorphic DNA regions in the EL population with 149 single nucleotide polymorphisms resulting in amino acid substitutions. Transcriptome analysis showed, in the EL population, significant up regulation of genes involved in protein synthesis, the cell cycle and cellular respiration, whereas the DNA repair pathway and photosynthesis were down regulated. Like other algae, EL cells accumulated neutral lipids under nitrogen depletion. Our work demonstrates transcriptome and genome-wide impacts of natural selection on algal cells and points to a useful strategy for strain improvement.

Analysis of the Genome of Cyanophora paradoxa: An Algal Model for Understanding Primary Endosymbiosis

Algae and plants rely on the plastid (e.g., chloroplast) to carry out photosynthesis. This organelle traces its origin to a cyanobacterium that was captured over a billion years ago by a single-celled protist. Three major photosynthetic lineages (the green algae and plants [Viridiplantae], red algae [Rhodophyta], and Glaucophyta) arose from this primary endosymbiotic event and are putatively united as the Plantae (also known as Archaeplastida). Glaucophytes comprise a handful of poorly studied species that retain ancestral features of the cyanobacterial endosymbiont such as a peptidoglycan cell wall. Testing the Plantae hypothesis and elucidating glaucophyte evolution has in the past been thwarted by the absence of complete genome data from these taxa. Furthermore, multigene phylogenetics has fueled controversy about the frequency of primary plastid acquisitions during eukaryote evolution because these approaches have generally failed to recover Plantae monophyly and often provide conflicting results. Here, we review some of the key insights about Plantae evolution that were gleaned from a recent analysis of a draft genome assembly from Cyanophora paradoxa (Glaucophyta). We present results that conclusively demonstrate Plantae monophyly. We also describe new insights that were gained into peptidoglycan biosynthesis in glaucophytes and the carbon concentrating mechanism (CCM) in C. paradoxa plastids.

Evidence for Widespread Exonic Small RNAs in the Glaucophyte Alga Cyanophora paradoxa

RNAi (RNA interference) relies on the production of small RNAs (sRNAs) from double-stranded RNA and comprises a major pathway in eukaryotes to restrict the propagation of selfish genetic elements. Amplification of the initial RNAi signal by generation of multiple secondary sRNAs from a targeted mRNA is catalyzed by RNA-dependent RNA polymerases (RdRPs). This phenomenon is known as transitivity and is particularly important in plants to limit the spread of viruses. Here we describe, using a genome-wide approach, the distribution of sRNAs in the glaucophyte alga Cyanophora paradoxa. C. paradoxa is a member of the supergroup Plantae (also known as Archaeplastida) that includes red algae, green algae, and plants. The ancient (>1 billion years ago) split of glaucophytes within Plantae suggests that C. paradoxa may be a useful model to learn about the early evolution of RNAi in the supergroup that ultimately gave rise to plants. Using next-generation sequencing and bioinformatic analyses we find that sRNAs in C. paradoxa are preferentially associated with mRNAs, including a large number of transcripts that encode proteins arising from different functional categories. This pattern of exonic sRNAs appears to be a general trend that affects a large fraction of mRNAs in the cell. In several cases we observe that sRNAs have a bias for a specific strand of the mRNA, including many instances of antisense predominance. The genome of C. paradoxa encodes four sequences that are homologous to RdRPs in Arabidopsis thaliana. We discuss the possibility that exonic sRNAs in the glaucophyte may be secondarily derived from mRNAs by the action of RdRPs. If this hypothesis is confirmed, then transitivity may have had an ancient origin in Plantae.

Secondary and Tertiary Endosymbiosis and Kleptoplasty

Alga is an informal name that refers to a diverse group of photosynthetic eukaryotes that have a polyphyletic origin in the tree of life. Although genomics has provided powerful tools for understanding the evolution of algal photosynthesis many issues remain unresolved. These include explaining the intermingling of plastid-lacking taxa such as ciliates and oomycetes among plastid-containing groups of chromalveolates. Does this pattern reflect a single ancient endosymbiosis in the chromalveolate ancestor followed by independent plastid losses or multiple secondary endosymbioses? Here we review current knowledge about chromalveolate evolution and phylogeny with a focus on secondary and tertiary endosymbiosis and survey recent genome-wide analyses to assess the potentially broad and lasting impacts of plastid transfer on eukaryote evolution. We assess the evidence for ‘footprints’ of photosynthetic pasts that remain even when the plastid is lost. These data comprise remnant algal genes in the nucleus of plastid-lacking taxa that have putatively originated via intracellular gene transfer from the former endosymbiont. We also provide a survey of recent work done in the field of protein import (i.e., via translocons) into chromalveolate and other plastids derived from secondary endoysmbiosis. We contrast the similarities and differences between primary and secondary plastid protein import machineries and speculate on the key innovations that led to their establishment. And finally, we take a careful look at the remarkable case of sea slug (Elysia chlorotica) kleptoplasty and photosynthesis and review recent work aimed at explaining this phenomenon in different metazoa. In particular, we critically assess support for the hypothesis that sea slug photosynthesis is explained by massive horizontal gene transfer (HGT) from the genome of the captured alga.