Genomic Footprints of a Cryptic Plastid Endosymbiosis in Diatoms

Moustafa, Ahmed; Beszteri, Bánk; Maier, Uwe G.; Bowler, Chris; Valentin, Klaus; Bhattacharya, Debashish

doi:10.1126/science.1172983

Cited by 373 publications

(388 citation statements)

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“…S1). Stramenopiles, on the other hand, represent a major lineage of eukaryotes that appeared following a secondary endosymbiosis event involving a heterotrophic exosymbiont host and algal endosymbionts 18,19 . Among these, diatoms constitute a highly successful and diversified group, with possibly over 10,000 extant species.…”

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

et al. 2013

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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.

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

et al. 2013

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“…S4B). Alternatively, like diatoms (22), prymnesiophytes may have obtained green-lineage genes from an ancient cryptic endosymbiont. Although the paucity of eukaryotic phytoplankton genomes may influence results, nuclear-encoded marker genes from larger cultured prymnesiophytes also show strong green-lineage affiliations (3).…”

Section: Resultsmentioning

confidence: 99%

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Cuvelier

Allen

Monier

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Among eukaryotes, four major phytoplankton lineages are responsible for marine photosynthesis; prymnesiophytes, alveolates, stramenopiles, and prasinophytes. Contributions by individual taxa, however, are not well known, and genomes have been analyzed from only the latter two lineages. Tiny "picoplanktonic" members of the prymnesiophyte lineage have long been inferred to be ecologically important but remain poorly characterized. Here, we examine pico-prymnesiophyte evolutionary history and ecology using cultivation-independent methods. 18S rRNA gene analysis showed picoprymnesiophytes belonged to broadly distributed uncultivated taxa. Therefore, we used targeted metagenomics to analyze uncultured pico-prymnesiophytes sorted by flow cytometry from subtropical North Atlantic waters. The data reveal a composite nuclear-encoded gene repertoire with strong green-lineage affiliations, which contrasts with the evolutionary history indicated by the plastid genome. Measured pico-prymnesiophyte growth rates were rapid in this region, resulting in primary production contributions similar to the cyanobacterium Prochlorococcus. On average, picoprymnesiophytes formed 25% of global picophytoplankton biomass, with differing contributions in five biogeographical provinces spanning tropical to subpolar systems. Elements likely contributing to success include high gene density and genes potentially involved in defense and nutrient uptake. Our findings have implications reaching beyond pico-prymnesiophytes, to the prasinophytes and stramenopiles. For example, prevalence of putative Ni-containing superoxide dismutases (SODs), instead of Fe-containing SODs, seems to be a common adaptation among eukaryotic phytoplankton for reducing Fe quotas in low-Fe modern oceans. Moreover, highly mosaic gene repertoires, although compositionally distinct for each major eukaryotic lineage, now seem to be an underlying facet of successful marine phytoplankton.comparative genomics | primary production | prymnesiophytes | marine photosynthesis | haptophytes G lobal primary production is partitioned equally among terrestrial and marine ecosystems, each accounting for ≈50 gigatons of carbon per year (1). The phytoplankton responsible for marine primary production include the cyanobacteria, Prochlorococcus and Synechococcus, and a multitude of eukaryotic phytoplankton, such as diatoms, dinoflagellates, prasinophytes, and prymnesiophytes (2-4). Most oceanic phytoplankton are "picoplanktonic" (<2-3 μm diameter) and have high surface area to volume ratios, an advantage in open-ocean low-nutrient conditions (5-8). 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 (9-11). The observed genomic divergence is associated with major differences in physiology and niche adaptation (10).Pigment-based estimates indicate that prymnesiophytes, also know...

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“…Quantification of these algal signatures has the potential to answer fundamental questions about the spread and secondary loss of plastids across the eukaryotic tree but has led to conflicting results. For example, a large and unexpected number of 'green' genes were found in the genomes of diatoms 32 and were interpreted to be evidence of a cryptic secondary endosymbiosis involving a green alga before the establishment of the red alga-derived plastid that diatoms currently harbour. However, these results were re-evaluated and found to be unconvincing 33 .…”

Section: Endosymbiotic Gene Transfer and Replacementmentioning

confidence: 99%

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

Curtis

Tanifuji

Burki

et al. 2012

Nature

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Genomic Footprints of a Cryptic Plastid Endosymbiosis in Diatoms

Abstract: Genomic Footprints of a Cryptic Plastid www.sciencemag.org (this information is current as of September 8, 2009 ):The following resources related to this article are available online at

Cited by 373 publications

References 22 publications

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

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

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

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