Insights into the role of DNA methylation in diatoms by genome-wide profiling in Phaeodactylum tricornutum.

DNA cytosine methylation is a widely conserved epigenetic mark in eukaryotes that appears to have critical roles in the regulation of genome structure and transcription. Genome-wide methylation maps have so far only been established from the supergroups Archaeplastida and Unikont. Here we report the first whole-genome methylome from a stramenopile, the marine model diatom Phaeodactylum tricornutum. Around 6% of the genome is intermittently methylated in a mosaic pattern. We find extensive methylation in transposable elements. We also detect methylation in over 320 genes. Extensive gene methylation correlates strongly with transcriptional silencing and differential expression under specific conditions. By contrast, we find that genes with partial methylation tend to be constitutively expressed. These patterns contrast with those found previously in other eukaryotes. By going beyond plants, animals and fungi, this stramenopile methylome adds significantly to our understanding of the evolution of DNA methylation in eukaryotes.

Transcription factor families inferred from genome sequences of photosynthetic stramenopiles.

• By comparative analyses we identify lineage-specific diversity in transcription factors (TFs) from stramenopile (or heterokont) genome sequences. We compared a pennate (Phaeodactylum tricornutum) and a centric diatom (Thalassiosira pseudonana) with those of other stramenopiles (oomycetes, Pelagophyceae, and Phaeophyceae (Ectocarpus siliculosus)) as well as to that of Emiliania huxleyi, a haptophyte that is evolutionarily related to the stramenopiles. • We provide a detailed description of diatom TF complements and report numerous peculiarities: in both diatoms, the heat shock factor (HSF) family is overamplified and constitutes the most abundant class of TFs; Myb and C2H2-type zinc finger TFs are the two most abundant TF families encoded in all the other stramenopile genomes investigated; the presence of diatom and lineage-specific gene fusions, in particular a class of putative photoreceptors with light-sensitive Per-Arnt-Sim (PAS) and DNA-binding (basic-leucine zipper, bZIP) domains and an HSF-AP2 domain fusion. • Expression data analysis shows that many of the TFs studied are transcribed and may be involved in specific responses to environmental stimuli. • Evolutionary and functional relevance of these observations are discussed.

Genome-wide analysis of the diatom cell cycle unveils a novel type of cyclins involved in environmental signaling.

BACKGROUND: Despite the enormous importance of diatoms in aquatic ecosystems and their broad industrial potential, little is known about their life cycle control. Diatoms typically inhabit rapidly changing and unstable environments, suggesting that cell cycle regulation in diatoms must have evolved to adequately integrate various environmental signals. The recent genome sequencing of Thalassiosira pseudonana and Phaeodactylum tricornutum allows us to explore the molecular conservation of cell cycle regulation in diatoms. RESULTS: By profile-based annotation of cell cycle genes, counterparts of conserved as well as new regulators were identified in T. pseudonana and P. tricornutum. In particular, the cyclin gene family was found to be expanded extensively compared to that of other eukaryotes and a novel type of cyclins was discovered, the diatom-specific cyclins. We established a synchronization method for P. tricornutum that enabled assignment of the different annotated genes to specific cell cycle phase transitions. The diatom-specific cyclins are predominantly expressed at the G1-to-S transition and some respond to phosphate availability, hinting at a role in connecting cell division to environmental stimuli. CONCLUSION: The discovery of highly conserved and new cell cycle regulators suggests the evolution of unique control mechanisms for diatom cell division, probably contributing to their ability to adapt and survive under highly fluctuating environmental conditions.

The Phaeodactylum genome reveals the evolutionary history of diatom genomes.

Diatoms are photosynthetic secondary endosymbionts found throughout marine and freshwater environments, and are believed to be responsible for around one-fifth of the primary productivity on Earth. The genome sequence of the marine centric diatom Thalassiosira pseudonana was recently reported, revealing a wealth of information about diatom biology. Here we report the complete genome sequence of the pennate diatom Phaeodactylum tricornutum and compare it with that of T. pseudonana to clarify evolutionary origins, functional significance and ubiquity of these features throughout diatoms. In spite of the fact that the pennate and centric lineages have only been diverging for 90 million years, their genome structures are dramatically different and a substantial fraction of genes ( approximately 40%) are not shared by these representatives of the two lineages. Analysis of molecular divergence compared with yeasts and metazoans reveals rapid rates of gene diversification in diatoms. Contributing factors include selective gene family expansions, differential losses and gains of genes and introns, and differential mobilization of transposable elements. Most significantly, we document the presence of hundreds of genes from bacteria. More than 300 of these gene transfers are found in both diatoms, attesting to their ancient origins, and many are likely to provide novel possibilities for metabolite management and for perception of environmental signals. These findings go a long way towards explaining the incredible diversity and success of the diatoms in contemporary oceans.

The evolution of introns in human duplicated genes.

In previous work [Jabbari, K., Rayko, E., Bernardi, G., 2003. The major shifts of human duplicated genes. Gene 317, 203-208], we investigated the fate of ancient duplicated genes after the compositional transitions that occurred between the genomes of cold- and warm-blooded vertebrates. We found that the majority of duplicated copies were transposed to the "ancestral genome core", the gene-dense genome compartment that underwent a GC enrichment at the compositional transitions. Here, we studied the consequences of the events just outlined on the introns of duplicated genes. We found that, while intron number was highly conserved, total intron size (the sum of intron sizes within any given gene) was smaller in the GC-rich copies compared to the GC-poor copies, especially in dispersed copies (i.e., copies located on different chromosomes or chromosome arms). GC-rich copies also showed higher densities of CpG islands and Alus, whereas GC-poor copies were characterized by higher densities of LINEs. The features of the copies that underwent the compositional transition and became GC-richer are suggestive of, or related to, functional changes.

The major shifts of human duplicated genes.

Since many gene duplications in the human genome are ancient duplications going back to the origin of vertebrates, the question may be asked about the fate of such duplicated genes at the compositional genome transitions that occurred between cold- and warm-blooded vertebrates. Indeed, at that transition, about half of the (GC-poor) genes of cold-blooded vertebrates (the genes of the gene-dense "ancestral genome core") underwent a GC enrichment to become the genes of the "genome core" of warm-blooded vertebrates. Since the compositional distribution of the human duplicated genes investigated (1111 pairs) mimics the general distribution of human genes (about 50% GC(3)-poor and 50% GC(3)-rich genes, the border being at 60% GC(3)), we considered two possibilities, namely that the compositional transition affected either (i) about half of the copies on a random basis, or (ii) preferentially only one copy of the duplicated genes. The two possibilities could be distinguished if each copy is put into one of two subsets according to its GC(3) level. Indeed, in the first case, the two distributions would be similar, whereas in the second case, the two distributions would be different, one copy having maintained the ancestral GC-poor composition, and one copy having undergone the compositional change. Using this approach, we could show that, by far and large, one copy of the duplicated genes preferentially underwent the GC enrichment. This result implies that this copy, which had possibly acquired a different function and/or regulation, was preferentially translocated into the gene-dense compartment of the genome, the "ancestral genome core", namely the "gene space" which underwent the compositional transition at the emergence of warm-blooded vertebrates.