Correction for Szul et al., “Carbon Fate and Flux in
            <i>Prochlorococcus</i>
            under Nitrogen Limitation”

Szul, Martin J.; Dearth, Stephen P.; Campagna, Shawn R.; Zinser, Erik R.

doi:10.1128/msystems.00204-19

Cited by 7 publications

(4 citation statements)

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“…6), Prochlorococcus was the numerically dominant sucrose-producing organism detected in these populations (Table 1). Prochlorococcus has strong diel gene expression for anabolic and catabolic processes (23) and is known to accumulate polysaccharides during the day, particularly under nitrogen limitation (68). If we assume that cellular quotas of sucrose in Prochlorococcus grown in culture are similar to those in the environment, Prochlorococcus alone could explain the sucrose concentrations seen in the environment (Fig.…”

Section: Discussionmentioning

confidence: 99%

Particulate Metabolites and Transcripts Reflect Diel Oscillations of Microbial Activity in the Surface Ocean

et al. 2021

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Light fuels photosynthesis and organic matter production by primary producers in the sunlit ocean. The quantity and quality of the organic matter produced influence community function, yet in situ measurements of metabolites, the products of cellular metabolism, over the diel cycle are lacking. We evaluated community-level biochemical consequences of oscillations of light in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter from 15 m every 4 h over 8 days. Total particulate metabolite concentration peaked at dusk and represented up to 2% of total particulate organic carbon (POC). The concentrations of 55/79 (70%) individual metabolites exhibited significant 24-h periodicity, with daily fold changes from 1.6 to 12.8, often greater than those of POC and flow cytometry-resolvable biomass, which ranged from 1.2 to 2.8. Paired metatranscriptome analysis revealed the taxa involved in production and consumption of a subset of metabolites. Primary metabolites involved in anabolism and redox maintenance had significant 24-h periodicity and diverse organisms exhibited diel periodicity in transcript abundance associated with these metabolites. Compounds with osmotic properties displayed the largest oscillations in concentration, implying rapid turnover and supporting prior evidence of functions beyond cell turgor maintenance. The large daily oscillation of trehalose paired with metatranscriptome and culture data showed that trehalose is produced by the nitrogen-fixing cyanobacterium Crocosphaera, likely to store energy for nighttime metabolism. Together, paired measurements of particulate metabolites and transcripts resolve strategies that microbes use to manage daily energy and redox oscillations and highlight dynamic metabolites with cryptic roles in marine microbial ecosystems. IMPORTANCE Fueled by light, phytoplankton produce the organic matter that supports ocean ecosystems and carbon sequestration. Ocean change impacts microbial metabolism with repercussions for biogeochemical cycling. As the small molecule products of cellular metabolism, metabolites often change rapidly in response to environmental conditions and form the basis of energy and nutrient management and storage within cells. By pairing measurements of metabolites and gene expression in the stratified surface ocean, we reveal strategies of microbial energy management over the day-night cycle and hypothesize that oscillating metabolites are important substrates for dark respiration by phytoplankton. These high-resolution diel measurements of in situ metabolite concentrations form the basis for future work into the specific roles these compounds play in marine microbial communities.

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Section: Discussionmentioning

confidence: 99%

Particulate Metabolites and Transcripts Reflect Diel Oscillations of Microbial Activity in the Surface Ocean

et al. 2021

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“…However, to our knowledge, we provide the first evidence of either the connection between the PPP and nucleic acid degradation or its connection to aromatic amino acid biosynthesis. Nucleoside enrichment patterns have been observed in other marine phytoplankton, as inosine was also enriched in N-stressed Prochlorococcus (Szul et al , 2019). Hence, similar metabolic dynamics may support other phytoplankton.…”

Section: Resultsmentioning

confidence: 81%

Harmful Algal Bloom-Forming Organism Responds to Nutrient Stress Distinctly From Model Phytoplankton

McLean

et al. 2021

Preprint

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Resources such as nitrogen (N) and phosphorus (P) play an important role in primary production and constraining phytoplankton bloom dynamics. Models to predict bloom dynamics require mechanistic knowledge of algal metabolic shifts in response to resource limitation. For well-studied model phytoplankton like diatoms, this information is plentiful. However, for less-studied groups such as the raphidophytes, there remain significant gaps in understanding metabolic changes associated with nutrient limitation. Using a novel combination of metabolomics and transcriptomics, we examined how the harmful algal bloom-forming raphidophyte Heterosigma akashiwo shifts its metabolism under N- and P-stress. We chose H. akashiwo because of its ubiquity within estuarine environments worldwide, where bloom dynamics are influenced by N and P availability. Our results show that each stress phenotype is distinct in both the allocation of carbon and the recycling of macromolecules. Further, we identified biomarkers of N- and P-stress that may be applied in situ to help modelers and stakeholders manage, predict, and prevent future blooms. These findings provide a mechanistic foundation to model the metabolic traits and trade-offs associated with N- and P-stress in H. akashiwo, and evaluate the extent to which these metabolic responses can be inferred in other phytoplankton groups.

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“…Because we infer the amount of extracellular C as the difference between TOC and cellular C estimated from cell counts, the released extracellular C could be in the form of dissolved organic C (DOC), but could also be in the form of vesicles, gels or transparent exopolymers (Biller et al 2014 a , b , c ; Iuculano et al 2017). Previous experimental studies where organic C release was measured in Prochlorococcus cultures using 14 C as a tracer suggested that 2–24% of the primary productivity is released as DOC (Bertilsson et al 2005; Lopez‐Sandoval et al 2013), although higher loss values have also been reported (up to ~ 60%, Szul et al 2019). Indirect assessments suggest that a somewhat higher fraction of the fixed carbon is lost from the cells, either as extracellular organic C or respired as CO 2 .…”

Section: Discussionmentioning

confidence: 99%

“…Secondly, significant information is available as to the physiological, transcriptomic and evolutionary responses of the cells to acute N starvation (e.g. Steglich et al 2001, Tolonen et al 2006, Gilbert and Fagan 2011, Szul et al 2019). Thirdly, long‐term analyses of batch cultures may identify cellular physiological processes not seen when cells are growing exponentially or exposed to sudden or short‐term nutrient starvation (e.g.…”

mentioning

confidence: 99%

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

Roth‐Rosenberg

Aharonovich

Omta

et al. 2021

Limnology & Oceanography

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Every living cell is composed of macromolecules such as proteins, DNA, RNA, and pigments. The ratio between these macromolecular pools depends on the allocation of resources within the organism to different physiological requirements, and in turn affects biogeochemical cycles of elements such as carbon, nitrogen, and phosphorus. Here, we present detailed measurements of the macromolecular composition of Prochlorococcus MIT9312, a representative strain of a globally abundant marine primary producer, as it grows and declines due to nitrogen starvation in laboratory batch cultures. As cells reached stationary stage and declined, protein per cell decreased by $ 30% whereas RNA per cell and pigments per cell decreased by $ 75%. The decline stage was associated with the appearance of chlorotic cells, which had higher forward scatter (a proxy for cell size) but lower chlorophyll autofluorescence, as well as with changes in photosynthetic pigment composition. Specifically, during culture decline divinyl-chlorophyll-like pigments emerged, which were not observed during exponential growth. These divinyl-chlorophyll-like pigments were also observed in natural samples from the Eastern Mediterranean. Over 90% of the carbon fixed by Prochlorococcus MIT9312 (but not of a different strain, NATL2A) was released into the growth media under these laboratory conditions. Variations in RNA/protein indicate that, broadly defined, the macromolecular composition of Prochlorococcus MIT9312 is more similar to eukaryotic phytoplankton than to marine heterotrophic bacteria, possibly due to the significant investment in photosynthetic machinery of phototrophs.

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Correction for Szul et al., “Carbon Fate and Flux in Prochlorococcus under Nitrogen Limitation”

Abstract: Page 4: In Fig. 1A, the unit of measurement on the y axis should be as shown here.

Cited by 7 publications

References 0 publications

Particulate Metabolites and Transcripts Reflect Diel Oscillations of Microbial Activity in the Surface Ocean

Particulate Metabolites and Transcripts Reflect Diel Oscillations of Microbial Activity in the Surface Ocean

Harmful Algal Bloom-Forming Organism Responds to Nutrient Stress Distinctly From Model Phytoplankton

Dynamic macromolecular composition and high exudation rates in Prochlorococcus

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