skip to main content


Title: High CO2 concentration and iron availability determine the metabolic inventory in an Emiliania huxleyi ‐dominated phytoplankton community
Summary

Ocean acidification (OA), a consequence of anthropogenic carbon dioxide (CO2) emissions, strongly impacts marine ecosystems. OA also influences iron (Fe) solubility, affecting biogeochemical and ecological processes. We investigated the interactive effects of CO2and Fe availability on the metabolome response of a natural phytoplankton community. Using mesocosms we exposed phytoplankton to ambient (390 μatm) or future CO2levels predicted for the year 2100 (900 μatm), combined with ambient (4.5 nM) or high (12 nM) dissolved iron (dFe). By integrating over the whole phytoplankton community, we assigned functional changes based on altered metabolite concentrations. Our study revealed the complexity of phytoplankton metabolism. Metabolic profiles showed three stages in response to treatments and phytoplankton dynamics. Metabolome changes were related to the plankton group contributing respective metabolites, explaining bloom decline and community succession. CO2and Fe affected metabolic profiles. Most saccharides, fatty acids, amino acids and many sterols significantly correlated with the high dFe treatment at ambientpCO2. High CO2lowered the abundance of many metabolites irrespective of Fe. However, sugar alcohols accumulated, indicating potential stress. We demonstrate that not only altered species composition but also changes in the metabolic landscape affecting the plankton community may change as a consequence of future high‐CO2oceans.

 
more » « less
NSF-PAR ID:
10453796
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
22
Issue:
9
ISSN:
1462-2912
Page Range / eLocation ID:
p. 3863-3882
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Dissolved iron (dFe) plays an important role in regulating marine productivity. In high nutrient, low chlorophyll regions (>33% of the global ocean), iron is the primary growth limiting nutrient, and elsewhere iron can regulate nitrogen fixation by diazotrophs. The link between iron availability and carbon export is strongly dependent on the phytoplankton iron quotas or cellular Fe:C ratios. This ratio varies by more than an order of magnitude in the open ocean and is positively correlated with ambient dFe concentrations in field observations. Representing Fe:C ratios within models is necessary to investigate how ocean carbon cycling will interact with perturbations to iron cycling in a changing climate. The Community Earth System Model ocean component was modified to simulate dynamic, group‐specific, phytoplankton Fe:C that varies as a function of ambient iron concentration. The simulated Fe:C ratios improve the representation of the spatial trends in the observed Fe:C ratios. The acclimation of phytoplankton Fe:C ratios dampens the biogeochemical response to varying atmospheric deposition of soluble iron, compared to a fixed Fe:C ratio. However, varying atmospheric soluble iron supply has first order impacts on global carbon and nitrogen fluxes and on nutrient limitation spatial patterns. Our results suggest that pyrogenic Fe is a significant dFe source that rivals mineral dust inputs in some regions. Changes in dust flux and iron combustion sources (anthropogenic and wildfires) will modify atmospheric Fe inputs in the future. Accounting for dynamic phytoplankton iron quotas is critical for understanding ocean biogeochemistry and projecting its response to variations in atmospheric deposition.

     
    more » « less
  2. Summary

    Foliar stomatal movements are critical for regulating plant water loss and gas exchange. Elevated carbon dioxide (CO2) levels are known to induce stomatal closure. However, the current knowledge onCO2signal transduction in stomatal guard cells is limited. Here we report metabolomic responses ofBrassica napusguard cells to elevatedCO2using three hyphenated metabolomics platforms: gas chromatography‐mass spectrometry (MS); liquid chromatography (LC)‐multiple reaction monitoring‐MS; and ultra‐high‐performanceLC‐quadrupole time‐of‐flight‐MS. A total of 358 metabolites from guard cells were quantified in a time‐course response to elevatedCO2level. Most metabolites increased under elevatedCO2, showing the most significant differences at 10 min. In addition, reactive oxygen species production increased and stomatal aperture decreased with time. Major alterations in flavonoid, organic acid, sugar, fatty acid, phenylpropanoid and amino acid metabolic pathways indicated changes in both primary and specialized metabolic pathways in guard cells. Most interestingly, the jasmonic acid (JA) biosynthesis pathway was significantly altered in the course of elevatedCO2treatment. Together with results obtained fromJAbiosynthesis and signaling mutants as well asCO2signaling mutants, we discovered thatCO2‐induced stomatal closure is mediated byJAsignaling.

     
    more » « less
  3. Abstract

    Modern observations indicate that variations in marine phytoplankton stoichiometry correlate with the boundaries of major surface waters. For example, phytoplankton in the oligotrophic subtropical gyres typically have much higher C:N:P ratios (i.e., higher C:P and higher N:P ratios) than those in eutrophic upwelling regions and polar regions. Such a spatial pattern points to nutrient availability as a key environmental driver of stochiometric flexibility. Environmental dependence of phytoplankton C:N:P opens unexplored possibilities for modifying the strength of the biological pump under different climate conditions. Here we present a power law formulation of C:N:P flexibility that is driven by nutrients, temperature, and light. We embed the formulation in a global ocean carbon cycle model with multiple phytoplankton types and explore biogeochemical implications under glacial conditions. We find three key controls on export C:N:P ratio: phytoplankton physiology and community structure as well as the balance in regional production at the global level. Glacial inputs of iron and sea ice expansion are important modifiers of these three controls. We also find that global export C:N:P increases substantially under glacial conditions, and this strongly buffers global carbon export against decrease and draws down approximately 20 μatm of atmospheric CO2. These results point to the importance of including phytoplankton C:N:P flexibility in a mix of mechanisms that drive atmospheric CO2over glacial‐interglacial time scale. Finally, our simulations indicate decoupling of nutrients, which may provide a resolution to the longstanding disagreement regarding nutrient utilization in the glacial Southern Ocean derived from different nutrient proxies.

     
    more » « less
  4. Abstract

    We present a new approach for quantifying the bioavailability of dissolved iron (dFe) to oceanic phytoplankton. Bioavailability is defined using an uptake rate constant (kin‐app) computed by combining data on: (a) Fe content of individual in situ phytoplankton cells; (b) concurrently determined seawater dFe concentrations; and (c) growth rates estimated from the PISCES model. We examined 930 phytoplankton cells, collected between 2002 and 2016 from 45 surface stations during 11 research cruises. This approach is only valid for cells that have upregulated their high‐affinity Fe uptake system, so data were screened, yielding 560 single cellkin‐appvalues from 31 low‐Fe stations. We normalizedkin‐appto cell surface area (S.A.) to account for cell‐size differences.

    The resulting bioavailability proxy (kin‐app/S.A.) varies among cells, but all values are within bioavailability limits predicted from defined Fe complexes. In situ dFe bioavailability is higher than model Fe‐siderophore complexes and often approaches that of highly available inorganic Fe′. Station averagedkin‐app/S.A. are also variable but show no systematic changes across location, temperature, dFe, and phytoplankton taxa. Given the relative consistency ofkin‐app/S.A. among stations (ca. five‐fold variation), we computed a grand‐averaged dFe availability, which upon normalization to cell carbon (C) yieldskin‐app/C of 42,200 ± 11,000 L mol C−1 d−1. We utilizekin‐app/C to calculate dFe uptake rates and residence times in low Fe oceanic regions. Finally, we demonstrate the applicability ofkin‐app/C for constraining Fe uptake rates in earth system models, such as those predicting climate mediated changes in net primary production in the Fe‐limited Equatorial Pacific.

     
    more » « less
  5. Abstract

    Calanus finmarchicuswere reared from eggs to adults at 12°C and 16°C with non‐limiting food in combination with ambient (600μatm) and high (1100μatm)pCO2. These conditions are likely to be encountered by the species at the southern margins of its biogeographical range by the end of the century. Dry weight (DW), carbon (C) and nitrogen (N) mass, oil‐sac volume (OSV), fatty acid composition (FA), and oxygen consumption rates (OCR) were measured on newly molted stage CV copepodites and recently molted adult females. By focusing our measurements on these precise events in the life cycle, we were able to obtain a more accurate comparison of growth and respiration across treatments. Copepods raised at 12°C had a significantly greater DW, OSV, and C and N mass than those raised at 16°C HighpCO2, independent of temperature, was associated with a further increase in the DW and C content of the copepods. Interactive effects of temperature andpCO2resulted in a larger OSV at low temperature and highpCO2. Mass‐specific respiration rates were significantly lower at lower temperatures and elevatedpCO2suggesting that the increase in mass (DW, C, and OSV) resulted from reduced metabolic cost. The composition of fatty acids in the copepods varied mainly with temperature. Two fatty acids varied withpCO2: 16:0 tended to decrease with higherpCO2and 18:3n−3 tended to increase with higherpCO2. These observations suggest that elevatedpCO2/lower pH in future oceans may have a beneficial effect onC. finmarchicus.

     
    more » « less