Physiological and Molecular Evidence that Environmental Changes Elicit Morphological Interconversion in the Model Diatom Phaeodactylum tricornutum

Martino, Alessandra De; Bartual, Ana; Willis, Anusuya; Meichenin, Agnès; Villazán, Beatriz; Maheswari, Uma; Bowler, Chris

doi:10.1016/j.protis.2011.02.002

Cited by 88 publications

(114 citation statements)

References 42 publications

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“…Unlike the other unicellular model organisms S. cerevisiae, Schizosaccharomyces pombe and Chlamydomonas reinhardtii, it has a small compact genome that displays all the key features of more complex genomes, such as DNA methylation, RNA interference and histone modifications. Furthermore, P. tricornutum has the peculiarity to be pleiomorphic as it can be found in the form of four different morphotypes: fusiform, oval, round and triradiate 44 . Significantly, morphotype transition occurs in response to specific environmental conditions such as salinity stress, temperature stress and nutrient limitation 44,45 .…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, P. tricornutum has the peculiarity to be pleiomorphic as it can be found in the form of four different morphotypes: fusiform, oval, round and triradiate 44 . Significantly, morphotype transition occurs in response to specific environmental conditions such as salinity stress, temperature stress and nutrient limitation 44,45 . Therefore, P. tricornutum also constitutes an excellent model to study the basis of epigenomic reprogramming events that lead to morphological variations in response to external stimuli, for example, to assess the influence on adaptive evolutionary processes of the increased susceptibility of methylated genes to mutation.…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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

et al. 2013

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“…In the cocultures of P. tricornutum with strain KarMa, we also obtained indications of an influence of the bacterium on the diatom when MMA served as the nitrogen source. There, the diatom cells exhibited an oval morphotype, which is indicative of stress effects, e.g., nitrogen stress (45)(46)(47). As a nitrogen source was apparently not limiting in the coculture, the stress response might rely on the presence of formaldehyde that was presumably released from strain KarMa in the course of oxidative deamination of MMA.…”

Section: Discussionmentioning

confidence: 99%

Interkingdom Cross-Feeding of Ammonium from Marine Methylamine-Degrading Bacteria to the Diatom Phaeodactylum tricornutum

Suleiman

Zecher

Yücel

et al. 2016

Appl Environ Microbiol

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Methylamines occur ubiquitously in the oceans and can serve as carbon, nitrogen, and energy sources for heterotrophic bacteria from different phylogenetic groups within the marine bacterioplankton. Diatoms, which constitute a large part of the marine phytoplankton, are believed to be incapable of using methylamines as a nitrogen source. As diatoms are typically associated with heterotrophic bacteria, the hypothesis came up that methylotrophic bacteria may provide ammonium to diatoms by degradation of methylamines. This hypothesis was investigated with the diatom Phaeodactylum tricornutum and monomethylamine (MMA) as the substrate. Bacteria supporting photoautotrophic growth of P. tricornutum with MMA as the sole nitrogen source could readily be isolated from seawater. Two strains, Donghicola sp. strain KarMa, which harbored genes for both monomethylamine dehydrogenase and the N methylglutamate pathway, and Methylophaga sp. strain M1, which catalyzed MMA oxidation by MMA dehydrogenase, were selected for further characterization. While strain M1 grew with MMA as the sole substrate, strain KarMa could utilize MMA as a nitrogen source only when, e.g., glucose was provided as a carbon source. With both strains, release of ammonium was detected during MMA utilization. In coculture with P. tricornutum, strain KarMa supported photoautotrophic growth with 2 mM MMA to the same extent as with the equimolar amount of NH 4 Cl. In coculture with strain M1, photoautotrophic growth of P. tricornutum was also supported, but to a much lower degree than by strain KarMa. This proof-of-principle study with a synthetic microbial community suggests that interkingdom cross-feeding of ammonium from methylaminedegrading bacteria is a contribution to phytoplankton growth which has been overlooked so far. IMPORTANCEInteractions between diatoms and heterotrophic bacteria are important for marine carbon cycling. In this study, a novel interaction is described. Bacteria able to degrade monomethylamine, which is a ubiquitous organic nitrogen compound in marine environments, can provide ammonium to diatoms. This interkingdom metabolite transfer enables growth under photoautotrophic conditions in coculture, which would not be possible in the respective monocultures. This proof-of-principle study calls attention to a so far overlooked contribution to phytoplankton growth. W ithin the marine phytoplankton, diatoms (Bacillariophyceae) contribute significantly to the phototrophic primary production in the oceans (1). Typically, pelagic as well as benthic diatoms are associated with heterotrophic bacteria, leading to organismic interactions that range from commensal to antagonistic relationships (2). As the concentration of dissolved organic carbon is usually low in the water column of the oceans, heterotrophic bacteria can obviously profit from these interactions by using organic substrates released by the photoautotrophic diatoms. This mainly commensal relationship has been known for a long time and led to the definition of the phycosphere ...

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“…The raw reads were trimmed for adaptor and low-quality sequences and then aligned to P. tricornutum's version 2.0 set of 10,402 filtered gene models (genome.jgi.doe.gov/Phatr2/Phatr2.info.html) using CLC Genomics Workbench (v6.02) (42). Functional metabolic assignment for the different gene models were done according to KEGG database (43), Diatomcyc database (www.diatomcyc.org), and published literature (44,45). Additional details on the data analysis can be found in SI Materials and Methods.…”

Section: Methodsmentioning

confidence: 99%

Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress

Levitan¹,

Dinamarca²,

Zelzion

et al. 2014

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

208

211

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Diatoms are unicellular algae that accumulate significant amounts of triacylglycerols as storage lipids when their growth is limited by nutrients. Using biochemical, physiological, bioinformatics, and reverse genetic approaches, we analyzed how the flux of carbon into lipids is influenced by nitrogen stress in a model diatom, Phaeodactylum tricornutum. Our results reveal that the accumulation of lipids is a consequence of remodeling of intermediate metabolism, especially reactions in the tricarboxylic acid and the urea cycles. Specifically, approximately one-half of the cellular proteins are cannibalized; whereas the nitrogen is scavenged by the urea and glutamine synthetase/glutamine 2-oxoglutarate aminotransferase pathways and redirected to the de novo synthesis of nitrogen assimilation machinery, simultaneously, the photobiological flux of carbon and reductants is used to synthesize lipids. To further examine how nitrogen stress triggers the remodeling process, we knocked down the gene encoding for nitrate reductase, a key enzyme required for the assimilation of nitrate. The strain exhibits 40-50% of the mRNA copy numbers, protein content, and enzymatic activity of the wild type, concomitant with a 43% increase in cellular lipid content. We suggest a negative feedback sensor that couples photosynthetic carbon fixation to lipid biosynthesis and is regulated by the nitrogen assimilation pathway. This metabolic feedback enables diatoms to rapidly respond to fluctuations in environmental nitrogen availability.lipid | metabolism | stress | NR | RNAi

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Physiological and Molecular Evidence that Environmental Changes Elicit Morphological Interconversion in the Model Diatom Phaeodactylum tricornutum

Cited by 88 publications

References 42 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

Interkingdom Cross-Feeding of Ammonium from Marine Methylamine-Degrading Bacteria to the Diatom Phaeodactylum tricornutum

Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress

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