Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium <i>Crocosphaera watsonii</i> WH 8501

Shi, Tianshu; Ilikchyan, Irina; Rabouille, Sophie; Zehr, Jonathan P.

doi:10.1038/ismej.2009.148

Cited by 99 publications

(113 citation statements)

References 66 publications

(75 reference statements)

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“…Cluster analysis revealed two major groups that include key photosystem or nitrogen fixation proteins with increased abundances during the day and night respectively. These experiments demonstrate that the diel cycling observed in the transcriptome of unicellular diazotrophs (21,22,32) manifests itself in large scale changes in the global proteome, where more than 20% of the measured proteins in the diel experiment showed diel variation. In both the day-night and diel experiments, the metalloenzymes involved in nitrogen fixation in Crocosphaera watsonii were among those with the most pronounced changes in abundance, being largely absent during the day and present at night (Figs 1B and 2, Fig.…”

Section: Resultsmentioning

confidence: 97%

“…Whereas Crocosphaera's distinct nocturnal nitrogenase activity is one of its defining characteristics in both laboratory and field studies (6,36), the fate of the nitrogenase protein complex during the light period has remained controversial due to the technical limitations of transcriptional and immunological methods, where transcripts do not measure protein abundance and immunological methods may not detect posttranslationally modified proteins (6,15,21,36,37). Using mass spectrometrybased analysis of multiple tryptic peptides from each protein, this study demonstrates the near complete degradation of the metalloenzymes from the nitrogenase complex and the partial degradation of certain iron-containing components of photosynthesis.…”

Section: Resultsmentioning

confidence: 99%

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Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii

Saito¹,

Bertrand²,

Dutkiewicz

et al. 2011

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

202

228

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The marine nitrogen fixing microorganisms (diazotrophs) are a major source of nitrogen to open ocean ecosystems and are predicted to be limited by iron in most marine environments. Here we use global and targeted proteomic analyses on a key unicellular marine diazotroph Crocosphaera watsonii to reveal large scale diel changes in its proteome, including substantial variations in concentrations of iron metalloproteins involved in nitrogen fixation and photosynthesis, as well as nocturnal flavodoxin production. The daily synthesis and degradation of enzymes in coordination with their utilization results in a lowered cellular metalloenzyme inventory that requires ∼40% less iron than if these enzymes were maintained throughout the diel cycle. This strategy is energetically expensive, but appears to serve as an important adaptation for confronting the iron scarcity of the open oceans. A global numerical model of ocean circulation, biogeochemistry and ecosystems suggests that Crocosphaera's ability to reduce its iron-metalloenzyme inventory provides two advantages: It allows Crocosphaera to inhabit regions lower in iron and allows the same iron supply to support higher Crocosphaera biomass and nitrogen fixation than if they did not have this reduced iron requirement.cyanobacteria | marine iron cycle | nitrogen cycle

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Section: Resultsmentioning

confidence: 97%

Section: Resultsmentioning

confidence: 99%

Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii

Saito¹,

Bertrand²,

Dutkiewicz

et al. 2011

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

202

228

View full text Add to dashboard Cite

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“…Yet, by applying high temporal sampling resolution and sequencing depth, we show that a significant fraction of the diverse heterotrophic diazotrophs present in such estuarine systems indeed occasionally expresses nifH. Cyanobacterial diazotrophs may exhibit diel patterns in nifH gene expression (for example, Shi et al, 2010). Sampling time can, therefore, have affected the relative proportions of transcripts from the respective functional types of diazotrophs in our data set.…”

Section: Discussionmentioning

confidence: 99%

Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries

et al. 2014

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Nitrogen (N) fixation is fueling planktonic production in a multitude of aquatic environments. In meso-and poly-haline estuaries, however, the contribution of N by pelagic N 2 fixation is believed to be insignificant due to the high input of N from land and the presumed absence of active N 2 -fixing organisms. Here we report N 2 fixation rates, nifH gene composition and nifH gene transcript abundance for key diazotrophic groups over 1 year in two contrasting, temperate, estuarine systems: Roskilde Fjord (RF) and the Great Belt (GB) strait. Annual pelagic N 2 fixation rates averaged 17 and 61 mmol N m À 2 per year at the two sites, respectively. In RF, N 2 fixation was mainly accompanied by transcripts related to heterotrophic (for example, Pseudomonas sp.) and photoheterotrophic bacteria (for example, unicellular diazotrophic cyanobacteria group A). In the GB, the first of two N 2 fixation peaks coincided with a similar nifH-expressing community as in RF, whereas the second peak was synchronous with increased nifH expression by an array of diazotrophs, including heterotrophic organisms as well as the heterocystous cyanobacterium Anabaena. Thus, we show for the first time that significant planktonic N 2 fixation takes place in mesohaline, temperate estuaries and that the importance of heterotrophic, photoheterotrophic and photosynthetic diazotrophs is clearly variable in space and time.

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“…The metatranscriptomics analysis was focused on the two populations that were well represented in the data sets. It should be noted that although the presence of Crocosphaera was anticipated, the unicellular cyanobacterium fixes N 2 at night (Mohr et al, 2010;Shi et al 2010a), and thus N 2 fixation gene transcripts from this population were not expected to be found in the morning samples.…”

Section: Discussionmentioning

confidence: 99%

Metatranscriptomics of N2-fixing cyanobacteria in the Amazon River plume

et al. 2014

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Biological N 2 fixation is an important nitrogen source for surface ocean microbial communities. However, nearly all information on the diversity and gene expression of organisms responsible for oceanic N 2 fixation in the environment has come from targeted approaches that assay only a small number of genes and organisms. Using genomes of diazotrophic cyanobacteria to extract reads from extensive meta-genomic and -transcriptomic libraries, we examined diazotroph diversity and gene expression from the Amazon River plume, an area characterized by salinity and nutrient gradients. Diazotroph genome and transcript sequences were most abundant in the transitional waters compared with lower salinity or oceanic water masses. We were able to distinguish two genetically divergent phylotypes within the Hemiaulus-associated Richelia sequences, which were the most abundant diazotroph sequences in the data set. Photosystem (PS)-II transcripts in Richelia populations were much less abundant than those in Trichodesmium, and transcripts from several Richelia PS-II genes were absent, indicating a prominent role for cyclic electron transport in Richelia. In addition, there were several abundant regulatory transcripts, including one that targets a gene involved in PS-I cyclic electron transport in Richelia. High sequence coverage of the Richelia transcripts, as well as those from Trichodesmium populations, allowed us to identify expressed regions of the genomes that had been overlooked by genome annotations. High-coverage genomic and transcription analysis enabled the characterization of distinct phylotypes within diazotrophic populations, revealed a distinction in a core process between dominant populations and provided evidence for a prominent role for noncoding RNAs in microbial communities.

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Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501

Cited by 99 publications

References 66 publications

Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii

Iron conservation by reduction of metalloenzyme inventories in the marine diazotroph Crocosphaera watsonii

Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries

Metatranscriptomics of N2-fixing cyanobacteria in the Amazon River plume

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