The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation

Abstract

The smallest known eukaryotes, at Ϸ1-m diameter, are Ostreococcus tauri and related species of marine phytoplankton. The genome of Ostreococcus lucimarinus has been completed and compared with that of O. tauri. This comparison reveals surprising differences across orthologous chromosomes in the two species from highly syntenic chromosomes in most cases to chromosomes with almost no similarity. Species divergence in these phytoplankton is occurring through multiple mechanisms acting differently on different chromosomes and likely including acquisition of new genes through horizontal gene transfer. We speculate that this latter process may be involved in altering the cell-surface characteristics of each species. In addition, the genome of O. lucimarinus provides insights into the unique metal metabolism of these organisms, which are predicted to have a large number of selenocysteine-containing proteins. Selenoenzymes are more catalytically active than similar enzymes lacking selenium, and thus the cell may require less of that protein. As reported here, selenoenzymes, novel fusion proteins, and loss of some major protein families including ones associated with chromatin are likely important adaptations for achieving a small cell size.green algae ͉ picoeukaryote ͉ genome evolution ͉ selenium ͉ synteny P hytoplankton living in the oceans perform nearly half of total global photosynthesis (1). Eukaryotic phytoplankton exhibit great diversity that contrasts with the lower apparent diversity of ecological niches available to them in aquatic ecosystems. This observation, know as the ''paradox of the plankton,'' has long puzzled biologists (2). By providing molecular level information on related species, genomics is poised to provide new insights into this paradox.Picophytoplankton, with cell diameters Ͻ2 m, play a significant role in major biogeochemical processes, primary productivity, and food webs, especially in oligotrophic waters. Within this size class, the smallest known eukaryotes are Ostreococcus tauri and related species. Although more similar to flattened spheres in shape, these organisms are Ϸ1 m in diameter (3, 4) and have been isolated or detected from samples of diverse geographical origins (5-8). They belong to the Prasinophyceae, an early diverging class within the green plant lineage, and have a strikingly simple cellular organization, with no cell wall or flagella, and with a single chloroplast and mitochondrion (4). Recent work has shown that small-subunit rDNA sequences of Ostreococcus from cultures and environmental samples cluster into four different clades that are likely distinct enough to represent different species (6, 9).Here we report on the gene content, genome organization, and deduced metabolic capacity of the complete genome of Ostreococcus sp. strain CCE9901 (7), a representative of surface-ocean adapted Ostreococcus, referred to here as Ostreococcus lucimarinus. We compare it to the analogous features of the related species O. tauri strain OTH95 (10). Our results show that many process...

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

“…We found high gene density in the pico-prymnesiophyte metagenome ( Fig. 3A and SI Materials and Methods, Section 7), akin to pico-prasinophytes, which purportedly underwent genome streamlining to optimize life in oligotrophic niches (9,11). GC content was 60%.…”

“…Despite the importance of eukaryotic phytoplankton to carbon cycling only six genomes have been sequenced and analyzed comparatively, all being from diatoms and prasinophytes. These revealed greater differentiation than anticipated on the basis of 18S rRNA gene analyses (9)(10)(11). The observed genomic divergence is associated with major differences in physiology and niche adaptation (10).…”

slr1923 of Synechocystis sp. PCC6803 Is Essential for Conversion of 3,8-Divinyl(proto)chlorophyll(ide) to 3-Monovinyl(proto)chlorophyll(ide)

“…The existence of a second vinyl reductase that has low or no homology to DVR was predicted by Nagata et al (2005), and Ito et al (2008) reached a similar conclusion from slr1923. Indeed, the slr1923 (cvrA) homolog was found in other cyanobacteria, in the red alga C. merolae (Matsuzaki et al, 2004), in the diatom T. pseudonana (Armbrust et al, 2004), and in the green algae O. lucimarinus (Palenik et al, 2007) and C. reinhardtii. The deduced amino acid sequences of the homologues of Slr1923 have no homology to that of DVR.…”

“…The significance of the presence of two copies in G. violaceus is not clear at the moment. It was found that the homolog is present not only in cyanobacteria but also in eukaryotic algae such as the red alga C. merolae 10D (CMJ076C; Matsuzaki et al, 2004), a diatom, Thalassiosira pseudonana CMP 1335 (gw1.2.195.1; Armbrust et al, 2004), and the green algae Ostreococcus lucimarinus (OSTLU_36251; Palenik et al, 2007) and Chlamydomonas reinhardtii (CHLRE-DRAFT_106754). Surprisingly, it is also found in land plants such as Arabidopsis (AT1G04620) and rice (Oryza sativa; 4335472).…”

Metatranscriptomic analysis of autonomously collected and preserved marine bacterioplankton

“…MS024-2A (Woyke et al, 2009) and eubacterium SCB49 (Yooseph et al, 2010). Ostreococcus (Derelle et al, 2006;Palenik et al, 2007) and Micromonas (Worden et al, 2009) were among the most abundant picoeukaryotes identified in annotated proteincoding transcripts, but rRNA-based analysis suggests a large diversity of eukaryotes without sequenced genomes were present in the samples.…”