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Stukel, MR, Kelly TB, Aluwihare LI, Barbeau KA, Goericke R, Krause JW, Landry MR, Ohman MD.  2019.  The Carbon:(234)Thorium ratios of sinking particles in the California current ecosystem 1: relationships with plankton ecosystem dynamics. Marine Chemistry. 212:1-15.   10.1016/j.marchem.2019.01.003   AbstractWebsite

We investigated variability in the C:Th-234 ratio of sinking particles and its relationship to changing water column characteristics and plankton ecological dynamics during 29 Lagrangian experiments conducted on six cruises of the California Current Ecosystem Long-Term Ecological Research (CCE-LTER) Program. C:Th-234 ratios of sinking particles collected by a surface-tethered sediment trap ((CThST)-Th-:234) varied from 2.3 to 20.5 mu mol C dpm(-1) over a depth range of 47-150 m. C:Th-234(ST) was significantly greater (by a factor of 1.8) than C:Th-234 ratios of suspended > 51-mu m particles collected in the same water parcels with in situ pumps. C:Th-234 ratios of large (> 200-mu m) sinking particles also exceeded those of smaller sinking particles. C:Th-234(ST) decreased with depth from the base of the euphotic zone through the upper twilight zone. C:Th-234(ST) was positively correlated with several indices of ecosystem productivity including particulate organic carbon (POC) and chlorophyll (Chl) concentrations, mesozooplankton biomass, and the fraction of Chl > 20-mu m. Principal component analysis and multiple linear regression suggested that decaying phytoplankton blooms exhibited higher C:Th-234(ST) than actively growing blooms at similar biomass levels. C:Th-234(ST) was positively correlated with indices of the fractional contribution of fecal pellets in sediment traps when the proportion of fecal pellets was low in the traps, likely because of a correlation between mesozooplankton biomass and other indices of ecosystem productivity. However, when fecal pellets were a more important component of sinking material, C:Th-234(ST) decreased with increasing fecal pellet content. C:Th-234(ST) was also positively correlated with the Si:C ratio of sinking particles. Across the dataset (and across depths) a strong correlation was found between C:Th-234(ST) and the ratio of vertically-integrated POC to vertically-integrated total water column Th-234 (C-v:Th-234(tot)). A mechanistic one-layer, two-box model of thorium sorption and desorption was invoked to explain this correlation. Two empirical models (one using C-v:Th-234(tot); one using depth and vertically-integrated Chl) were developed to predict C:Th-234 ratios in this coastal upwelling biome. The former regression (log(10)(C:Th-234(ST)) = 0.43 x log(10)(C-v:Th-234(tot)) + 0.53) was found to also be a reasonable predictor for C:Th-234(ST) from diverse regions including the Southern Ocean, Sargasso Sea, Subarctic North Pacific, and Eastern Tropical North Pacific.

Stukel, MR, Aluwihare LI, Barbeau KA, Chekalyuk AM, Goericke R, Miller AJ, Ohman MD, Ruacho A, Song H, Stephens BM, Landry MR.  2017.  Mesoscale ocean fronts enhance carbon export due to gravitational sinking and subduction. Proceedings of the National Academy of Sciences of the United States of America. 114:1252-1257.   10.1073/pnas.1609435114   AbstractWebsite

Enhanced vertical carbon transport (gravitational sinking and subduction) at mesoscale ocean fronts may explain the demonstrated imbalance of new production and sinking particle export in coastal upwelling ecosystems. Based on flux assessments from U-238:Th-234 disequilibrium and sediment traps, we found 2 to 3 times higher rates of gravitational particle export near a deep-water front (305 mg C.m(-2).d(-1)) compared with adjacent water or to mean (nonfrontal) regional conditions. Elevated particle flux at the front wasmechanistically linked to Fe-stressed diatoms and high-mesozooplankton fecal pellet production. Using a data assimilative regional ocean model fit to measured conditions, we estimate that an additional similar to 225 mg C.m(-2).d(-1) was exported as subduction of particle-rich water at the front, highlighting a transport mechanism that is not captured by sediment traps and is poorly quantified by most models and in situ measurements. Mesoscale fronts may be responsible for over a quarter of total organic carbon sequestration in the California Current and other coastal upwelling ecosystems.

Stuart, RK, Bundy R, Buck K, Ghassemain M, Barbeau K, Palenik B.  2017.  Copper toxicity response influences mesotrophic Synechococcus community structure. Environmental Microbiology. 19:756-769.   10.1111/1462-2920.13630   AbstractWebsite

Picocyanobacteria from the genus Synechococcus are ubiquitous in ocean waters. Their phylogenetic and genomic diversity suggests ecological niche differentiation, but the selective forces influencing this are not well defined. Marine picocyanobacteria are sensitive to Cu toxicity, so adaptations to this stress could represent a selective force within, and between, species', also known as clades. Here, we compared Cu stress responses in cultures and natural populations of marine Synechococcus from two co-occurring major mesotrophic clades (I and IV). Using custom microarrays and proteomics to characterize expression responses to Cu in the lab and field, we found evidence for a general stress regulon in marine Synechococcus. However, the two clades also exhibited distinct responses to copper. The Clade I representative induced expression of genomic island genes in cultures and Southern California Bight populations, while the Clade IV representative downregulated Fe-limitation proteins. Copper incubation experiments suggest that Clade IV populations may harbour stress-tolerant subgroups, and thus fitness tradeoffs may govern Cu-tolerant strain distributions. This work demonstrates that Synechococcus has distinct adaptive strategies to deal with Cu toxicity at both the clade and subclade level, implying that metal toxicity and stress response adaptations represent an important selective force for influencing diversity within marine Synechococcus populations.

Semeniuk, DM, Bundy RM, Payne CD, Barbeau KA, Maldonado MT.  2015.  Acquisition of organically complexed copper by marine phytoplankton and bacteria in the northeast subarctic Pacific Ocean. Marine Chemistry. 173:222-233.   10.1016/j.marchem.2015.01.005   AbstractWebsite

Copper (Cu) is an essential micronutrient for marine phytoplankton, but can cause toxicity at elevated intracellular concentrations. The majority of Cu (>99.9%) in oceanic surface waters is bound to strong organic ligands, presumably produced by prokaryotes to detoxify Cu. Although laboratory studies have demonstrated that organically complexed Cu may be bioavailable to marine eukaryotic phytoplankton, the bioavailability of Cu organic complexes to indigenous marine phytoplankton has not been examined in detail. Using the carrier free radioisotope Cu-67 at an iron limited station in the northeast subarctic Pacific Ocean, we performed size fractionated short-term Cu uptake assays with three Cu(II)-chelates, and Cu-67 bound to the strong in situ ligands, with or without additions of weak Cu(I) ligands. Estimates of the maximum supply of inorganic Cu (Cu') to the cell surface of eukaryotic phytoplankton were unable to account for the observed Cu uptake rates from the in situ ligands and two of the three added Cu(II)-chelates. Addition of 10 nM weak organic Cu(I) ligands enhanced uptake of Cu bound to the in situ ligands. Thus, Cu within the in situ and strong artificial Cu(II) organic ligands was accessible to the phytoplankton community via various possible Cu uptake strategies, including; cell surface enzymatically mediated reduction of Cu(II) to Cu(I), the substrate of the high-affinity Cu transport system in eukaryotes; or ligand exchange between weak Cu-binding ligands and the cellular Cu transporters. During a 14-hour uptake assay, particulate Cu concentrations reached a plateau in most treatments. Losses were observed in some treatments, especially in the small size fractions (<5 mu m), corresponding with faster initial Cu uptake rates. This may indicate that Cu cycling is rapid between particulate and dissolved phases due to cellular efflux or remineralization by micrograzers. The acquisition of Cu from the strong in situ ligands puts into question the historic role attributed to Cu binding ligands in decreasing Cu bioavailability. (C) 2015 Elsevier B.V. All rights reserved.

Semeniuk, DM, Bundy RM, Posacka AM, Robert M, Barbeau KA, Maldonado MT.  2016.  Using 67Cu to study the biogeochemical cycling of copper in the northeast subarctic Pacific Ocean. Frontiers in Marine Science. 3:78.   10.3389/fmars.2016.00078   Abstract

Microbial copper (Cu) nutrition and dissolved Cu speciation were surveyed along Line P, a coastal to open ocean transect that extends from the coast of British Columbia, Canada, to the high-nutrient-low-chlorophyll (HNLC) zone of the northeast subarctic Pacific Ocean. Steady-state size fractionated Cu uptake rates and Cu:C assimilation ratios were determined at in situ Cu concentrations and speciation using a 67Cu tracer method. The cellular Cu:C ratios that we measured (~30 µmol Cu mol C-1) are similar to recent estimates using synchrotron x-ray fluorescence (SXRF), suggesting that the 67Cu method can determine in situ metabolic Cu demands. We examined how environmental changes along the Line P transect influenced Cu metabolism in the sub-microplankton community. Cellular Cu:C assimilation ratios and uptake rates were compared with net primary productivity, bacterial abundance and productivity, total dissolved Cu, Cu speciation, and a suite of other chemical and biological parameters. Total dissolved Cu concentrations ([Cu]d) were within a narrow range (1.46 to 2.79 nM), and Cu was bound to a ~5-fold excess of strong ligands with conditional stability constants ( ) of ~1014. Free Cu2+ concentrations were low (pCu 14.4 to 15.1), and total and size fractionated net primary productivity (NPPV; µg C L-1 d-1) were negatively correlated with inorganic Cu concentrations ([Cu′]). We suggest this is due to greater Cu′ drawdown by faster growing phytoplankton populations. Using the relationship between [Cu′] drawdown and NPPV, we calculated a regional photosynthetic Cu:C drawdown export ratio between 1.5 and 15 µmol Cu mol C-1, and a mixed layer residence time (2.5 to 8 years) that is similar to other independent estimates (2-12 years). Total particulate Cu uptake rates were between 22 and 125 times faster than estimates of Cu export; this is possibly mediated by rapid cellular Cu uptake and efflux by phytoplankton and bacteria or the effects of grazers and bacterial remineralization on dissolved Cu. These results provide a more detailed understanding of the interactions between Cu speciation and microorganisms in seawater, and present evidence that marine phytoplankton modify Cu speciation in the open ocean.

Semeniuk, DM, Taylor RL, Bundy RM, Johnson WK, Cullen JT, Robert M, Barbeau KA, Maldonado MT.  2016.  Iron-copper interactions in iron-limited phytoplankton in the northeast subarctic Pacific Ocean. Limnology and Oceanography. 61:279-297.   10.1002/lno.10210   AbstractWebsite

In August 2010, iron (Fe) and Fe and copper (Cu) addition incubation experiments were conducted at two low Fe stations (P20 and P26) along Line P, off the western coast of British Columbia, to investigate Cu physiology in Fe- and Fe-light co-limited phytoplankton. Chlorophyll a concentrations ([Chl a]), maximum variable fluorescence yield (F-v/F-m), and Fe uptake rates by the Cu-dependent high-affinity Fe transport system (HAFeTS) were measured. Additions of Fe resulted in an increase in [Chl a] and F-v/F-m at both stations compared with the controls, regardless of light availability, and confirmed that the phytoplankton communities were Fe-limited. Uptake of Fe by the HAFeTS in both incubations increased with the addition of Fe, and likely reflects luxury Fe uptake and storage. While the in situ inorganic Cu concentrations were similar to those that can induce Cu-limitation in laboratory cultures, increasing Cu availability had no effect on biomass accumulation during both incubations, regardless of Fe availability or light regime. At P26, additions of 1 nmol L-1 CuSO4 resulted in a short-term increase in F-v/F-m of the phytoplankton community, and an increase in Fe uptake rates by large phytoplankton (>5 mu m), but only when light was not limiting. These data confirm a complex interaction between light, Fe and Cu physiology in indigenous phytoplankton communities, and suggest that these interactions may be both spatially heterogeneous and different for different phytoplankton size classes.