Effect of PAR irradiance intensity on Phaeocystis antarctica (Prymnesiophyceae) growth and DMSP, DMSO, and acrylate concentrations.

Phaeocystis antarctica forms extensive spring blooms in the Southern Ocean that coincide with high concentrations of dimethylsulfoniopropionate (DMSP), dimethylsulfoxide (DMSO), dimethylsulfide (DMS), and acrylate. We determined how concentrations of these compounds changed during the growth of axenic P. antarctica cultures exposed to light-limiting, sub-saturating, and saturating PAR irradiances. Cellular DMSP concentrations per liter cell volume (CV) ranged between 199 and 403 mmol · LCV -1 , with the highest concentrations observed under light-limiting PAR. Cellular acrylate concentrations did not change appreciably with a change in irradiance level or growth, ranging between 18 and 45 mmol · LCV -1 , constituting an estimated 0.2%-2.8% of cellular carbon. Both dissolved acrylate and DMSO increased substantially with irradiance during exponential growth on a per-cell basis, ranging from 0.91 to 3.15 and 0.24 to 1.39 fmol · cell-1 , respectively, indicating substantial export of these compounds into the dissolved phase. Average cellular DMSO:DMSP ratios increased 7.6-fold between exponential and stationary phases of batch growth, with a 3- to 13-fold increase in cellular DMSO likely formed from abiotic reactions of DMSP and DMS with reactive oxygen species (ROS). At mM levels, cellular DMSP and acrylate are proposed to serve as de facto antioxidants in P. antarctica not regulated by oxidative stress or changes in ROS. Instead, cellular DMSP concentrations are likely controlled by other physiological processes including an overflow mechanism to remove excess carbon via acrylate, DMS, and DMSO during times of unbalanced growth brought on by physical stress or nutrient limitation. Together, these compounds should aid P. antarctica in adapting to a range of PAR irradiances by maintaining cellular functions and reducing oxidative stress.

Photochemical Production and Photolysis of Acrylate in Seawater.

The marine organosulfur cycle has been studied intensively for over 30 years motivated by the hypothesis that dimethylsulfide (DMS) affects Earth's radiation balance and climate. The main source of DMS is from the enzymatic lysis of dimethylsulfoniopropionate (DMSP), the latter of which is a significant component of carbon, sulfur, and energy fluxes in the oceans. Acrylate is also produced during DMSP lysis, but unlike DMS or DMSP, very little is known about the marine acrylate cycle. Herein, a new source of acrylate was identified in seawater as a product formed from the photolysis of dissolved organic matter (DOM). Photochemical production rates varied from 1.6 to 5.0 pM (µmol quanta cm-2)-1, based on photon exposures determined from nitrite actinometry. A positive correlation (r = 0.87) was observed between acrylate photoproduction and the seawater absorption coefficient at 330 nm. Acrylate photoproduction was initiated by UV radiation, with UV-B and UV-A contributing approximately 32 and 68% to the total production, respectively. Acrylate did not photolyze in high-purity water or seawater at concentrations less than 100 nM. These findings improve our understanding of the role that sunlight plays in the marine acrylate cycle, a reactive form of DOM that significantly affects the carbon cycle and ecology of the upper ocean.

Oceanic efflux of ancient marine dissolved organic carbon in primary marine aerosol.

Breaking waves produce bubble plumes that burst at the sea surface, injecting primary marine aerosol (PMA) highly enriched with marine organic carbon (OC) into the atmosphere. It is widely assumed that this OC is modern, produced by present-day biological activity, even though nearly all marine OC is thousands of years old, produced by biological activity long ago. We used natural abundance radiocarbon (14C) measurements to show that 19 to 40% of the OC associated with freshly produced PMA was refractory dissolved OC (RDOC). Globally, this process removes 2 to 20 Tg of RDOC from the oceans annually, comparable to other RDOC losses. This process represents a major removal pathway for old OC from the sea, with important implications for oceanic and atmospheric biogeochemistry, the global carbon cycle, and climate.

Properties of Seawater Surfactants Associated with Primary Marine Aerosol Particles Produced by Bursting Bubbles at a Model Air-Sea Interface.

Surfactants account for minor fractions of total organic carbon in the ocean but can significantly influence the production of primary marine aerosol particles (PMA) at the sea surface via modulation of bubble surface tension. During September and October 2016, model PMA (mPMA) were produced from seawater by bursting bubbles at two biologically productive and two oligotrophic stations in the western North Atlantic Ocean. Total concentrations of surfactants extracted from mPMA and seawater were quantified and characterized via measurements of surface tension isotherms and critical micelle concentrations (CMCs). Surfactant CMCs in biologically productive seawater were lower than those in the oligotrophic seawater suggesting that surfactant mixtures in the two regions were chemically distinct. mPMA surfactants were enriched in all regions relative to those in the associated seawater. Surface tension isotherms indicate that mPMA surfactants were weaker than corresponding seawater surfactants. mPMA from biologically productive seawater contained higher concentrations of surfactants than those produced from oligotrophic seawater, supporting the hypothesis that seawater surfactant properties modulate mPMA surfactant concentrations. Diel variability in concentrations of seawater and mPMA surfactants in some regions is consistent with biological and/or photochemical processing. This work demonstrates direct links between surfactants in mPMA and those in the associated seawater.

Concentrations and Photochemistry of Acetaldehyde, Glyoxal, and Methylglyoxal in the Northwest Atlantic Ocean.

The photochemical production and degradation of acetaldehyde, glyoxal, and methylglyoxal along with spatiotemporal variations in their concentrations were investigated in the Northwest Atlantic Ocean from September to October 2016. Surface seawater concentrations did not exhibit day-night differences and ranged from 1.0-7.1, 1.4-4.8, and 0.25-2.8 nmol L-1 for acetaldehyde, glyoxal, and methylglyoxal, respectively. Higher glyoxal and methylglyoxal concentrations were observed in biologically productive seawater from Georges Bank and coastal Rhode Island compared to the oligotrophic Sargasso Sea, whereas no differences were seen in acetaldehyde concentrations among these stations. Carbonyl photoproduction rates in surface seawater ranged from 0.35-0.79, 0.06-0.2, and 0.02-0.07 nmol L-1 h-1 for acetaldehyde, glyoxal, and methylglyoxal, respectively. Methylglyoxal slowly photodegraded in seawater (∼0.001-0.03 nmol L-1 h-1), whereas acetaldehyde and glyoxal were photochemically stable. Photochemical sources explained from ∼7 to 53% of the estimated total production of acetaldehyde in the surface mixed layer; a similar estimate could not be determined for glyoxal or methylglyoxal, since several processes have not been quantified that potentially affect their concentrations. Our results suggest that acetaldehyde is likely supersaturated in surface seawater relative to its typical atmospheric concentrations, whereas glyoxal and methylglyoxal are significantly undersaturated.

The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle.

Algae produce massive amounts of dimethylsulfoniopropionate (DMSP), which fuel the organosulfur cycle1,2. On a global scale, several petagrams of this sulfur species are produced annually, thereby driving fundamental processes and the marine food web1. An important DMSP transformation product is dimethylsulfide, which can be either emitted to the atmosphere3,4 or oxidized to dimethylsulfoxide (DMSO) and other products5. Here we report the discovery of a structurally unusual metabolite, dimethylsulfoxonium propionate (DMSOP), that is synthesized by several DMSP-producing microalgae and marine bacteria. As with DMSP, DMSOP is a low-molecular-weight zwitterionic metabolite that carries both a positively and a negatively charged functional group. Isotope labelling studies demonstrate that DMSOP is produced from DMSP, and is readily metabolized to DMSO by marine bacteria. DMSOP was found in near nanomolar amounts in field samples and in algal culture media, and thus represents-to our knowledge-a previously undescribed biogenic source for DMSO in the marine environment. The estimated annual oceanic production of oxidized sulfur from this pathway is in the teragram range, similar to the calculated dimethylsulfide flux to the atmosphere3. This sulfoxonium metabolite is therefore a key metabolite of a previously undescribed pathway in the marine sulfur cycle. These findings highlight the importance of DMSOP in the marine organosulfur cycle.

Modelling dimethylsulfide diffusion in the algal external boundary layer: implications for mutualistic and signalling roles.

Dimethylsulfide (DMS), a dominant organic sulfur species in the surface ocean, may act as a signalling molecule and contribute to mutualistic interactions between bacteria and marine algae. These proposed functions depend on the DMS concentration in the vicinity of microorganisms. Here, we modelled the DMS enrichment at the surface of DMS-releasing marine algal cells as a function of DMS production rate, algal cell radius and turbulence. Our results show that the DMS concentration at the surface of unstressed phytoplankton with low DMS production rates can be enriched by <1 nM, whereas for mechanically stressed algae with high activities of the enzyme DMSP-lyase (a coccolithophore and a dinoflagellate) DMS cell surface enrichments can reach ~10 nM, and could potentially reach µM levels in large cells. These DMS enrichments are much higher than the median DMS concentration in the surface ocean (1.9 nM), and thus may attract and support the growth of bacteria living in the phycosphere. The bacteria in turn may provide photoactive iron chelators (siderophores) that enhance algal iron uptake and provide algal growth factors such as auxins and vitamins. The present study highlights new insights on the extent and impact of microscale DMS enrichments at algal surfaces, thereby contributing to our understanding of the potential chemoattractant and mutualistic roles of DMS in marine microorganisms.

Carbonate Disequilibrium in the External Boundary Layer of Freshwater Chrysophytes: Implications for Contaminant Uptake.

The interplay between biological and chemical reactions in the freshwater phytoplankton phycosphere and the resulting modulations of contaminant speciation and uptake is poorly characterized. Here we modeled the effect of algal C and N uptake on carbonate cycling and speciation of selected contaminants in the phycosphere (external boundary layer) of chrysophytes, a key phytoplankton group in oligotrophic systems. We calculated an enrichment in H+ concentration relative to that in the bulk solution (pH 7.0) of approximately 40% or a depletion of approximately 30% for NH4+ or NO3--grown cells, respectively, at the algal membrane surface of a 5-µm radius cell. Such changes are mainly due to direct H+ uptake or release at the plasmalemma if NO3- or NH4+ is the N source, respectively. Due to these pH changes in the external boundary layer, competition between H+ and metals for uptake is enhanced, for NH4+-grown cells which contributes to a decrease in potential metal uptake. Our model suggests that the uptake of protonated weakly acidic organic acids (HA) is greater in NH4+-grown cells compared to that in NO3--grown cells. The account of chemical reactions in the algal external boundary layer could improve ecological risk assessments for a wide range of contaminants.

Wavelength- and Temperature-Dependent Apparent Quantum Yields for Photochemical Production of Carbonyl Compounds in the North Pacific Ocean.

Photolysis of dissolved organic matter is the main source of carbonyl compounds in sunlit seawater, but rates and photoefficiences are poorly constrained. Wavelength- and temperature-dependent apparent quantum yields (AQYs) were determined for photochemical production of acetaldehyde, glyoxal, and methylglyoxal in North Pacific Ocean seawater. Wavelength-dependent AQYs at 20 °C decreased exponentially with increasing wavelength between 290 and 380 nm, from 1.29 × 10-4 to 4.12 × 10-6, 2.52 × 10-5 to 6.89 × 10-7, and 4.37 × 10-6 to 1.25 × 10-7 mol (mol quanta)-1 for acetaldehyde, glyoxal, and methylglyoxal, respectively. AQYs decreased after 6 h irradiation at 310 nm, possibly due to depletion of photochemical precursors or carbonyl photolysis. Average activation energies (95% CI) for photochemical production at 320 nm were 9.31 (±9.3), 26.0 (±7.5), and 34.7 (±12.8) kJ mol-1 for acetaldehyde, glyoxal, and methylglyoxal, respectively. The peak response for photochemical production rates in surface seawater was ∼325 nm, with ∼30% contribution from UV-B and ∼70% from UV-A. Computed noontime wavelength-integrated photoproduction rates were 0.5-0.8, 0.04-0.2, and 0.03-0.06 nmol L-1 h-1 for acetaldehyde, glyoxal, and methylglyoxal, respectively, under cloudless conditions in August. Results can be used to determine regional-scale photochemical production rates for these compounds in the surface ocean.

CDOM Sources and Photobleaching Control Quantum Yields for Oceanic DMS Photolysis.

Photolysis is a major removal pathway for the biogenic gas dimethylsulfide (DMS) in the surface ocean. Here we tested the hypothesis that apparent quantum yields (AQY) for DMS photolysis varied according to the quantity and quality of its photosensitizers, chiefly chromophoric dissolved organic matter (CDOM) and nitrate. AQY compiled from the literature and unpublished studies ranged across 3 orders of magnitude at the 330 nm reference wavelength. The smallest AQY(330) were observed in coastal waters receiving major riverine inputs of terrestrial CDOM (0.06-0.5 m3 (mol quanta)-1). In open-ocean waters, AQY(330) generally ranged between 1 and 10 m3 (mol quanta)-1. The largest AQY(330), up to 34 m3 (mol quanta)-1), were seen in the Southern Ocean potentially associated with upwelling. Despite the large AQY variability, daily photolysis rate constants at the sea surface spanned a smaller range (0.04-3.7 d-1), mainly because of the inverse relationship between CDOM absorption and AQY. Comparison of AQY(330) with CDOM spectral signatures suggests there is an interplay between CDOM origin (terrestrial versus marine) and photobleaching that controls variations in AQYs, with a secondary role for nitrate. Our results can be used for regional or large-scale assessment of DMS photolysis rates in future studies.

Carbon Monoxide Photoproduction from Particles and Solutes in the Delaware Estuary under Contrasting Hydrological Conditions.

Full-spectrum, ultraviolet (UV), and visible broadband apparent quantum yields (AQYs) for carbon monoxide (CO) photoproduction from chromophoric dissolved organic matter (CDOM) and particulate organic matter (POM) were determined in the Delaware Estuary in two hydrologically contrasting seasons in 2012: an unusually low flow in August and a storm-driven high flow in November. Average AQYs for CDOM and POM in November were 10 and 16 times the corresponding AQYs in August. Maximum AQYs in November occurred in a midestuary particle absorption maximum zone. Although POM AQYs were generally smaller than CDOM AQYs, the ratio of the former to the latter increased substantially from the UV to the visible. In both seasons, UV solar radiation was the primary driver for CO photoproduction from CDOM whereas visible light was the principal contributor to POM-based CO photoproduction. CDOM dominated CO photoproduction in the uppermost water layer while POM prevailed at deeper depths. On a depth-integrated basis, the Delaware Estuary shifted from a CDOM-dominated system in August to a POM-dominated system in November with respect to CO photoproduction. This study reveals that flood events may enhance photochemical cycling of terrigenous organic matter and switch the primary photochemical driver from CDOM to POM.

Evidence for the mutual effects of dimethylsulfoniopropionate and nitric oxide during the growth of marine microalgae.

Dimethylsulfoniopropionate (DMSP) and nitric oxide (NO) in marine microalgae are considered as two important compounds involved in a variety of physiological functions. We examined the NO responses and the growth of Isochrysis galbana Parke and Gymnodinium sp. when supplemented with different concentrations of DMSP solutions in the cultures. Production of DMSP and dimethylsulfide (DMS) in Amphidinium carterae and Emiliania Huxleyi was investigated after the addition of NO donor sodium nitroprusside (SNP) and NO solution to algal media. The release peaks of NO were observed in cell suspensions of I. galbana Parke and Gymnodinium sp. immediately after the injection of DMSP solutions. The growth of these two microalgae was found to be significantly promoted or inhibited caused by exogenous DMSP. There was a decrease of DMSP concentrations in algal cultures within 24 h, accompanied with an increase in DMS, due to the effect of NO. The results provided direct evidence to confirm that there exist mutual effects of DMSP and NO during the growth of marine microalgae, which is speculated to be related to their roles as signaling molecules in planktonic communities.

Wavelength and temperature-dependent apparent quantum yields for photochemical formation of hydrogen peroxide in seawater.

Wavelength and temperature-dependent apparent quantum yields (AQYs) were determined for the photochemical production of hydrogen peroxide using seawater obtained from coastal and oligotrophic stations in Antarctica, the Pacific Ocean at Station ALOHA, the Gulf of Mexico, and at several sites along the East Coast of the United States. For all samples, AQYs decreased exponentially with increasing wavelength at 25 °C, ranging from 4.6 × 10(-4) to 10.4 × 10(-4) at 290 nm to 0.17 × 10(-4) to 0.97 × 10(-4) at 400 nm. AQYs for different seawater samples were remarkably similar irrespective of expected differences in the composition and concentrations of metals and dissolved organic matter (DOM) and in prior light exposure histories; wavelength-dependent AQYs for individual seawater samples differed by less than a factor of two relative to respective mean AQYs. Temperature-dependent AQYs increased between 0 and 35 °C on average by a factor of 1.8 per 10 °C, consistent with a thermal reaction (e.g., superoxide dismutation) controlling H2O2 photochemical production rates in seawater. Taken together, these results suggest that the observed poleward decrease in H2O2 photochemical production rates is mainly due to corresponding poleward decreases in irradiance and temperature and not spatial variations in the composition and concentrations of DOM or metals. Hydrogen peroxide photoproduction AQYs and production rates were not constant and not independent of the photon exposure as has been implicitly assumed in many published studies. Therefore, care should be taken when comparing and interpreting published H2O2 AQY or photochemical production rate results. Modeled depth-integrated H2O2 photochemical production rates were in excellent agreement with measured rates obtained from in situ free-floating drifter experiments conducted during a Gulf of Maine cruise, with differences (ca. 10%) well within measurement and modeling uncertainties. Results from this study provide a comprehensive data set of wavelength and temperature-dependent AQYs to model and remotely sense hydrogen peroxide photochemical production rates globally.

Effect of humic substance photodegradation on bacterial growth and respiration in lake water.

This study addresses how humic substance (HS) chemical composition and photoreactivity affect bacterial growth, respiration, and growth efficiency (BGE) in lake water. Aqueous solutions of HSs from diverse aquatic environments representing different dissolved organic matter sources (autochthonous and allochthonous) were exposed to artificial solar UV radiation. These solutions were added to lake water passed through a 0.7-microm-pore-size filter (containing grazer-free lake bacteria) followed by dark incubation for 5, 43, and 65 h. For the 5-h incubation, several irradiated HSs inhibited bacterial carbon production (BCP) and this inhibition was highly correlated with H2O2 photoproduction. The H2O2 decayed in the dark, and after 43 h, nearly all irradiated HSs enhanced BCP (average 39% increase relative to nonirradiated controls, standard error = 7.5%, n = 16). UV exposure of HSs also increased bacterial respiration (by approximately 18%, standard error = 5%, n = 4), but less than BCP, resulting in an average increase in BGE of 32% (standard error = 10%, n = 4). Photoenhancement of BCP did not correlate to HS bulk properties (i.e., elemental and chemical composition). However, when the photoenhancement of BCP was normalized to absorbance, several trends with HS origin and extraction method emerged. Absorbance-normalized hydrophilic acid and humic acid samples showed greater enhancement of BCP than hydrophobic acid and fulvic acid samples. Furthermore, absorbance-normalized autochthonous samples showed approximately 10-fold greater enhancement of BCP than allochthonous-dominated samples, indicating that the former are more efficient photoproducers of biological substrates.