Current sampling of genomic sequence data from eukaryotes is relatively poor, biased, and inadequate to address important questions about their biology, evolution, and ecology; this Community Page describes a resource of 700 transcriptomes from marine microbial eukaryotes to help understand their role in the world's oceans.
The introduction of plastids into different heterotrophic protists created lineages of algae that diversified explosively, proliferated in marine and freshwater environments, and radically altered the biosphere. The origins of these secondary plastids are usually inferred from the presence of additional plastid membranes. However, two examples provide unique snapshots of secondaryendosymbiosis-in-action, because they retain a vestige of the endosymbiont nucleus known as the nucleomorph. These are chlorarachniophytes and cryptomonads, which acquired their plastids from a green and red alga respectively. To allow comparisons between them, we have sequenced the nucleomorph genome from the chlorarachniophyte Bigelowiella natans: at a mere 373,000 bp and with only 331 genes, the smallest nuclear genome known and a model for extreme reduction. The genome is eukaryotic in nature, with three linear chromosomes containing densely packed genes with numerous overlaps. The genome is replete with 852 introns, but these are the smallest introns known, being only 18, 19, 20, or 21 nt in length. These pygmy introns are shown to be miniaturized versions of normal-sized introns present in the endosymbiont at the time of capture. Seventeen nucleomorph genes encode proteins that function in the plastid. The other nucleomorph genes are housekeeping entities, presumably underpinning maintenance and expression of these plastid proteins. Chlorarachniophyte plastids are thus serviced by three different genomes (plastid, nucleomorph, and host nucleus) requiring remarkable coordination and targeting. Although originating by two independent endosymbioses, chlorarachniophyte and cryptomonad nucleomorph genomes have converged upon remarkably similar architectures but differ in many molecular details that reflect two distinct trajectories to hypercompaction and reduction.plastid ͉ secondary endosymbiosis ͉ intron ͉ endosymbiosis T he origin of plastids through endosymbiosis of a cyanobacterium-like prokaryote transferred photosynthesis into eukaryotes and launched a massive wave of diversification that subsequently generated a tremendous range of algae and plants (1). This initial event is referred to as primary endosymbiosis ( Fig. 1) and created a plastid with two membranes such as those of green algae, plants, red algae, and glaucophyte algae (1). Transfer of genes from the endosymbiont to the nuclear genome of the host initially led to dependence of the endosymbiont on the host that was necessary to stabilize the partnership (2). Ongoing transfer has resulted in reduction of the prokaryotic genome, so that plastid DNA now represents probably Ͻ10% of its original gene content, and increasingly sophisticated regulation of the endosymbiont by the host has resulted in endosymbiont replication, gene expression, metabolic activity, and even death being managed by the eukaryotic host (3). Indeed, primary plastids seem to retain some autonomy only in the synthesis and deployment of redox proteins involved in photosynthetic electron transfer (4).A...
Proteorhodopsins are light-driven proton pumps involved in widespread phototrophy. Discovered in marine proteobacteria just 10 years ago, proteorhodopsins are now known to have been spread by lateral gene transfer across diverse prokaryotes, but are curiously absent from eukaryotes. In this study, we show that proteorhodopsins have been acquired by horizontal gene transfer from bacteria at least twice independently in dinoflagellate protists. We find that in the marine predator Oxyrrhis marina, proteorhodopsin is indeed the most abundantly expressed nuclear gene and its product localizes to discrete cytoplasmic structures suggestive of the endomembrane system. To date, photosystems I and II have been the only known mechanism for transducing solar energy in eukaryotes; however, it now appears that some abundant zooplankton use this alternative pathway to harness light to power biological functions.
Mitochondria are eukaryotic organelles that originated from an endosymbiotic α-proteobacterium. As an adaptation to maximize ATP production through oxidative phosphorylation, mitochondria contain inner membrane invaginations called cristae. Recent work has characterized a multi-protein complex in yeast and animal mitochondria called MICOS (mitochondrial contact site and cristae organizing system), responsible for the determination and maintenance of cristae [1-4]. However, the origin and evolution of these characteristic mitochondrial features remain obscure. We therefore conducted a comprehensive search for MICOS components across the major groups that encompass eukaryotic diversity to determine the extent of conservation of this complex. We detected homologs for the majority of MICOS components among opisthokonts (the group containing animals and fungi), but only Mic60 and Mic10 were consistently identified outside this group. The conservation of Mic60 and Mic10 in eukaryotes is consistent with their central role in MICOS function [5-7], indicating that the basic mechanism for cristae determination arose early in evolution and has remained relatively unchanged. We found that eukaryotes with ultrastructurally simplified anaerobic mitochondria that lack cristae have also lost MICOS. We then searched for a prokaryotic MICOS and identified a homolog of Mic60 present only in α-proteobacteria, providing evidence for the endosymbiotic origin of mitochondrial cristae. Our study clarifies the origins of mitochondrial cristae and their subsequent evolutionary history, provides evidence for a general mechanism of cristae formation and maintenance in eukaryotes, and points to a new potential factor involved in membrane differentiation in prokaryotes.
The origin of land plants from algae is a long-standing question in evolutionary biology. It is becoming increasingly clear that many characters that were once assumed to be 'embryophyte specific' can in fact be found in their closest algal relatives, the streptophyte algae. One such case is the phenylpropanoid pathway. While biochemical data indicate that streptophyte algae harbor lignin-like components, the phenylpropanoid core pathway, which serves as the backbone of lignin biosynthesis, has been proposed to have arisen at the base of the land plants. Here we revisit this hypothesis using a wealth of new sequence data from streptophyte algae. Tracing the biochemical pathway towards lignin biogenesis, we show that most of the genes required for phenylpropanoid synthesis and the precursors for lignin production were already present in streptophyte algae. Nevertheless, phylogenetic analyses and protein structure predictions of one of the key enzyme classes in lignin production, cinnamyl alcohol dehydrogenase (CAD), suggest that CADs of streptophyte algae are more similar to sinapyl alcohol dehydrogenases (SADs). This suggests that the end-products of the pathway leading to lignin biosynthesis in streptophyte algae may facilitate the production of lignin-like compounds and defense molecules. We hypothesize that streptophyte algae already possessed the genetic toolkit from which the capacity to produce lignin later evolved in vascular plants.
Microsporidian genomes are extraordinary among eukaryotes for their extreme reduction: although they are similar in form to other eukaryotic genomes, they are typically smaller than many prokaryotic genomes. At the same time, their rates of sequence evolution are among the highest for eukaryotic organisms. To explore the effects of compaction on nuclear genome evolution, we sequenced 685,000 bp of the Antonospora locustae genome (formerly Nosema locustae) and compared its organization with the recently completed genome of the human parasite Encephalitozoon cuniculi. Despite being very distantly related, the genomes of these two microsporidian species have retained an unexpected degree of synteny: 13% of genes are in the same context, and 30% of the genes were separated by a small number of short rearrangements. Microsporidian genomes are, therefore, paradoxically composed of rapidly evolving sequences harbored within a slowly evolving genome, although these two processes are sometimes considered to be coupled. Microsporidian genomes show that eukaryotic genomes (like genes) do not evolve in a clock-like fashion, and genome stability may result from compaction in addition to a lack of recombination, as has been traditionally thought to occur in bacterial and organelle genomes.
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