High single‐cell diversity in carbon and nitrogen assimilations by a chain‐forming diatom across a century

Olofsson, Malin; Kourtchenko, Olga; Zetsche, Eva‐Maria; Marchant, Hannah K.; Whitehouse, Martin J.; Godhe, Anna; Ploug, Helle

doi:10.1111/1462-2920.14434

Cited by 23 publications

(28 citation statements)

References 41 publications

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“…2017, Olofsson et al. 2019a). The evolution of various DIN transporters in diatoms, including high affinity transporters for vacuolar accumulation of NO 3 − , is considered to be key for the global dominance of these organisms in the ocean (Busseni et al.…”

Section: Discussionmentioning

confidence: 99%

“…An N‐specific hypothetical doubling time was then calculated from the excess ratio according to Olofsson et al. 's (2019a) equation 3 (Klawonn et al. , Bergkvist et al.…”

Section: Methodsmentioning

confidence: 99%

“…, Ellegaard and Ribeiro , Olofsson et al. 2019a). However, the mechanisms by which resting stages remain ready to resume vegetative growth after decades in the sediment are poorly known.…”

mentioning

confidence: 98%

“…, Olofsson et al. ,b). Using this approach, we examined potential uptake of inorganic C and N from the ambient environment and their assimilation within Skeletonema resting stages during long‐term (ca.…”

mentioning

confidence: 99%

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Resting Stages of Skeletonema marinoi Assimilate Nitrogen From the Ambient Environment Under Dark, Anoxic Conditions

Stenow

Olofsson

Robertson

et al. 2020

Journal of Phycology

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The planktonic marine diatom Skeletonema marinoi forms resting stages, which can survive for decades buried in aphotic, anoxic sediments and resume growth when re‐exposed to light, oxygen, and nutrients. The mechanisms by which they maintain cell viability during dormancy are poorly known. Here, we investigated cell‐specific nitrogen (N) and carbon (C) assimilation and survival rate in resting stages of three S. marinoi strains. Resting stages were incubated with stable isotopes of dissolved inorganic N (DIN), in the form of 15N‐ammonium (NH4+) or ‐nitrate (NO3−) and dissolved inorganic C (DIC) as 13C‐bicarbonate (HCO3−) under dark and anoxic conditions for 2 months. Particulate C and N concentration remained close to the Redfield ratio (6.6) during the experiment, indicating viable diatoms. However, survival varied between <0.1% and 47.6% among the three different S. marinoi strains, and overall survival was higher when NO3− was available. One strain did not survive in the NH4+ treatment. Using secondary ion mass spectrometry (SIMS), we quantified assimilation of labeled DIC and DIN from the ambient environment within the resting stages. Dark fixation of DIC was insignificant across all strains. Significant assimilation of 15N‐NO3− and 15N‐NH4+ occurred in all S. marinoi strains at rates that would double the nitrogenous biomass over 77–380 years depending on strain and treatment. Hence, resting stages of S. marinoi assimilate N from the ambient environment at slow rates during darkness and anoxia. This activity may explain their well‐documented long survival and swift resumption of vegetative growth after dormancy in dark and anoxic sediments.

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Section: Discussionmentioning

confidence: 99%

“…An N‐specific hypothetical doubling time was then calculated from the excess ratio according to Olofsson et al. 's (2019a) equation 3 (Klawonn et al. , Bergkvist et al.…”

Section: Methodsmentioning

confidence: 99%

“…, Ellegaard and Ribeiro , Olofsson et al. 2019a). However, the mechanisms by which resting stages remain ready to resume vegetative growth after decades in the sediment are poorly known.…”

mentioning

confidence: 98%

mentioning

confidence: 99%

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Resting Stages of Skeletonema marinoi Assimilate Nitrogen From the Ambient Environment Under Dark, Anoxic Conditions

Stenow

Olofsson

Robertson

et al. 2020

Journal of Phycology

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“…Diatoms can consume this low amount of nitrate and encounter the nitrogen limitation stage in a few days. This kind of setup for the nitrogen limitation experiment has been used in previous studies in which the starting nitrate concentration ranged from 50 to 100 M (15,27,(40)(41)(42)(43)(44). The measurements of nitrate consumption and cell growth both indicate that the nitrogen-limited condition was reached at day 4 in the low-nitrogen treatment ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Responses of Marine Diatom Skeletonema marinoi to Nutrient Deficiency: Programmed Cell Death

Wang

Chen

et al. 2020

Appl Environ Microbiol

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Diatoms are important phytoplankton and contribute greatly to the primary productivity of marine ecosystems. Despite the ecological significance of diatoms and the importance of programmed cell death (PCD) in the fluctuation of diatom populations, little is known about the molecular mechanisms of PCD triggered by different nutrient stresses. Here we describe the physiological, morphological, biochemical, and molecular changes in response to low levels of nutrients in the ubiquitous diatom Skeletonema marinoi. The levels of gene expression involved in oxidation resistance and PCD strongly increased upon nitrogen (N) or phosphorus (P) starvation. The enzymatic activity of caspase 3-like protein also increased. Differences in mRNA levels and protein activities were observed between the low-N and low-P treatments, suggesting that PCD could have a differential response to different nutrient stresses. When cultures were replete with N or P, the growth inhibition stopped. Meanwhile, the enzymatic activity of caspase 3-like protein and the number of cells with damaged membranes decreased. These results suggest that PCD is an important cell fate decision mechanism in the marine diatom S. marinoi. Our results provide important insight into how diatoms adjust phenotypic and genotypic features of their cell-regulated death programs when stressed by nutrient limitations. Overall, this study could allow us to better understand the molecular mechanism behind the formation and termination of diatom blooms in the marine environment. IMPORTANCE Our study showed how the ubiquitous diatom S. marinoi responded to different nutrient limitations with PCD in terms of physiological, morphological, biochemical, and molecular characteristics. Some PCD-related genes (PDCD4, GOX, and HSP90) induced by N deficiency were relatively upregulated compared to those induced by P deficiency. In contrast, the expression of the TSG101 gene in S. marinoi showed a clear and constant increase during P limitation compared to N limitation. These findings suggest that PCD is a complex mechanism involving several different proteins. The systematic mRNA level investigations provide new insight into understanding the oxidative stress- and cell death-related functional genes of diatoms involved in the response to nutrient fluctuations (N or P stress) in the marine environment.

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Consistent cell‐specific carbon fixation rates by small eukaryotic phytoplankton in contrasting nutrient‐limited conditions

Ong,

Gutiérrez‐Rodríguez,

Safi

et al. 2024

Limnology & Oceanography

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Small phytoplankton, consisting of pico and nano size fractions, are diverse in size and taxonomy. Yet, the differences in their productivity and taxonomic diversity are poorly described. Here, we measured the cell‐specific carbon fixation rates of picocyanobacteria Synechococcus, picoeukaryote, and nanoeukaryote populations, while unveiling their taxonomic composition in oligotrophic subtropical and high‐nutrient low‐chlorophyll subantarctic waters. We coupled 24 h in situ radiolabeled 14C incubations to flow cytometry sorting and DNA metabarcoding from the same incubated samples, offering a direct account of the community associated with the carbon fixation rates measured. In both water masses, nanoeukaryotes had the highest cell‐specific carbon fixation rate, followed by picoeukaryotes and Synechococcus (2.24 ± 29.99, 2.18 ± 2.08, and 0.78 ± 0.55 fgC cell−1 h−1, respectively). The cell‐specific carbon fixation rates and growth rates of Synechococcus were threefold higher in subtropical compared to subantarctic waters, while the rates of picoeukaryotes and nanoeukaryotes had no significant difference between the biogeochemically‐contrasting water masses. Sorted picoeukaryote populations were dominated by Mamiellophyceae, Pelagophyceae, Prymnesiophyceae, and Chrysophyceae, while nanoeukaryote populations were dominated by Dinophyceae and Prymnesiophyceae. Despite significant differences in their taxonomic composition, the sorted picoeukaryote populations in subantarctic waters and nanoeukaryote populations in subtropical and subantarctic waters were dominated by taxa reported in the literature as able to engage in phago‐mixotrophic strategies (Prymnesiophyceae, Chrysophyceae, and Dinophyceae), suggesting that such trophic strategy might be applied by discrete small photosynthetic eukaryote populations to alleviate macronutrient and iron stress.

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High single‐cell diversity in carbon and nitrogen assimilations by a chain‐forming diatom across a century

Cited by 23 publications

References 41 publications

Resting Stages of Skeletonema marinoi Assimilate Nitrogen From the Ambient Environment Under Dark, Anoxic Conditions

Resting Stages of Skeletonema marinoi Assimilate Nitrogen From the Ambient Environment Under Dark, Anoxic Conditions

Responses of Marine Diatom Skeletonema marinoi to Nutrient Deficiency: Programmed Cell Death

Consistent cell‐specific carbon fixation rates by small eukaryotic phytoplankton in contrasting nutrient‐limited conditions

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