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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.

C
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.

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Dupont, CL, McCrow JP, Valas R, Moustafa A, Walworth N, Goodenough U, Roth R, Hogle SL, Bai J, Johnson ZI, Mann E, Palenik B, Barbeau KA, Craig Venter J, Allen AE.  2015.  Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities. ISME J. 9:1076-1092.: International Society for Microbial Ecology   10.1038/ismej.2014.198   Abstract

Transitions in community genomic features and biogeochemical processes were examined in surface and subsurface chlorophyll maximum (SCM) microbial communities across a trophic gradient from mesotrophic waters near San Diego, California to the oligotrophic Pacific. Transect end points contrasted in thermocline depth, rates of nitrogen and CO2 uptake, new production and SCM light intensity. Relative to surface waters, bacterial SCM communities displayed greater genetic diversity and enrichment in putative sulfur oxidizers, multiple actinomycetes, low-light-adapted Prochlorococcus and cell-associated viruses. Metagenomic coverage was not correlated with transcriptional activity for several key taxa within Bacteria. Low-light-adapted Prochlorococcus, Synechococcus, and low abundance gamma-proteobacteria enriched in the>3.0-[mu]m size fraction contributed disproportionally to global transcription. The abundance of these groups also correlated with community functions, such as primary production or nitrate uptake. In contrast, many of the most abundant bacterioplankton, including SAR11, SAR86, SAR112 and high-light-adapted Prochlorococcus, exhibited low levels of transcriptional activity and were uncorrelated with rate processes. Eukaryotes such as Haptophytes and non-photosynthetic Aveolates were prevalent in surface samples while Mamielles and Pelagophytes dominated the SCM. Metatranscriptomes generated with ribosomal RNA-depleted mRNA (total mRNA) coupled to in vitro polyadenylation compared with polyA-enriched mRNA revealed a trade-off in detection eukaryotic organelle and eukaryotic nuclear origin transcripts, respectively. Gene expression profiles of SCM eukaryote populations, highly similar in sequence identity to the model pelagophyte Pelagomonas sp. CCMP1756, suggest that pelagophytes are responsible for a majority of nitrate assimilation within the SCM.

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Pizeta, I, Sander SG, Hudson RJM, Omanovic D, Baars O, Barbeau KA, Buck KN, Bundy RM, Carrasco G, Croot PL, Garnier C, Gerringa LJA, Gledhill M, Hirose K, Kondo Y, Laglera LM, Nuester J, Rijkenberg MJA, Takeda S, Twining BS, Wells M.  2015.  Interpretation of complexometric titration data: An intercomparison of methods for estimating models of trace metal complexation by natural organic ligands. Marine Chemistry. 173:3-24.   10.1016/j.marchem.2015.03.006   AbstractWebsite

With the common goal of more accurately and consistently quantifying ambient concentrations of free metal ions and natural organic ligands in aquatic ecosystems, researchers from 15 laboratories that routinely analyze trace metal speciation participated in an intercomparison of statistical methods used to model their most common type of experimental dataset, the complexometric titration. All were asked to apply statistical techniques that they were familiar with to model synthetic titration data that are typical of those obtained by applying state-of-the-art electrochemical methods - anodic stripping voltammetry (ASV) and competitive ligand equilibration-adsorptive cathodic stripping voltammetry (CLE-ACSV) - to the analysis of natural waters. Herein, we compare their estimates for parameters describing the natural ligands, examine the accuracy of inferred ambient free metal ion concentrations (]M-f]), and evaluate the influence of the various methods and assumptions used on these results. The ASV-type titrations were designed to test each participant's ability to correctly describe the natural ligands present in a sample when provided with data free of measurement error, i.e., random noise. For the three virtual samples containing just one natural ligand, all participants were able to correctly identify the number of ligand classes present and accurately estimate their parameters. For the four samples containing two or three ligand classes, a few participants detected too few or too many classes and consequently reported inaccurate 'measurements' of ambient [M-f]. Since the problematic results arose from human error rather than any specific method of analyzing the data, we recommend that analysts should make a practice of using one's parameter estimates to generate simulated (back-calculated) titration curves for comparison to the original data. The root-mean-squared relative error between the fitted observations and the simulated curves should be comparable to the expected precision of the analytical method and upon visual inspection the distribution of residuals should not be skewed. Modeling the synthetic, CLE-ACSV-type titration dataset, which comprises 5 titration curves generated at different analytical-windows or levels of competing ligand added to the virtual sample, proved to be more challenging due to the random measurement error that was incorporated. Comparison of the submitted results was complicated by the participants' differing interpretations of their task. Most adopted the provided 'true' instrumental sensitivity in modeling the CLE-ACSV curves, but several estimated sensitivities using internal calibration, exactly as is required for actual samples. Since most fitted sensitivities were biased low, systematic error in inferred ambient [M-f] and in estimated weak ligand (L-2) concentrations resulted. The main distinction between the mathematical approaches taken by participants lies in the functional form of the speciation model equations, with their implicit definition of independent and dependent or manipulated variables. In 'direct modeling', the dependent variable is the measured [M-f] (or I-p) and the total metal concentration ([M](T)) is considered independent In other, much more widely used methods of analyzing titration data - classical linearization, best known as van den Berg/Ruzic and isotherm fitting by nonlinear regression, best known as the langmuir or Gerringa methods - [M-f] is defined as independent and the dependent variable calculated from both [M](T) and [M-f]. Close inspection of the biases and variability in the estimates of ligand parameters and in predictions of ambient [M-f] revealed that the best results were obtained by the direct approach. Linear regression of transformed data yielded the largest bias and greatest variability, while non-linear isotherm fitting generated results with mean bias comparable to direct modeling, but also with greater variability. Participants that performed a unified analysis of ACSV titration curves at multiple detection windows for a sample improved their results regardless of the basic mathematical approach taken. Overall, the three most accurate sets of results were obtained using direct modeling of the unified multiwindow dataset, while the single most accurate set of results also included simultaneous calibration. We therefore recommend that where sample volume and time permit, titration experiments for all natural water samples be designed to include two or more detection windows, especially for coastal and estuarine waters. It is vital that more practical experimental designs for multi-window titrations be developed. Finally, while all mathematical approaches proved to be adequate for some datasets, matrix-based equilibrium models proved to be most naturally suited for the most challenging cases encountered in this work, i.e., experiments where the added ligand in ACSV became titrated. The ProMCC program (Omanovic et al., this issue) as well as the Excel Add-in based KINETEQL Multiwindow Solver spreadsheet (Hudson, 2014) have this capability and have been made available for public use as a result of this intercomparison exercise. (C) 2015 The Authors. Published by Elsevier B.V.

N
Dupont, CL, Barbeau K, Palenik B.  2008.  Ni uptake and limitation in marine Synechococcus strains. Applied and Environmental Microbiology. 74:23-31.   10.1128/aem.01007-07   AbstractWebsite

Ni accumulation and utilization were studied in two strains of marine Synechococcus, isolated from both coastal (CC9311; clade I) and open-ocean (WTH8102; clade III) environments, for which complete genome sequences are available. Both strains have genes encoding an Ni-containing urease and when grown on urea without Ni become Ni-N colimited. The Ni requirements of these strains also depend upon the genomic complement of genes encoding superoxide dismutase (SOD). WH8102, with a gene encoding only an Ni-SOD, has a novel obligate requirement for Ni, regardless of the N source. Reduced SOD activity in Ni-depleted cultures of VM8102 supports the link of this strain's Ni requirement to Ni-SOD. The genome of CC9311 contains a gene for a Cu/Zn-SOD in addition to a predicted pair of Ni-SODs, yet this strain cannot grow without Ni on NO3- and can grow only slowly on NH4+ without Ni, implying that the Cu/Zn-SOD cannot completely replace Ni-SOD in marine cyanobacteria. CC9311 does have a greater tolerance for Ni starvation. Both strains increase their Ni uptake capabilities and actively bioconcentrate Ni in response to decreasing extracellular and intracellular Ni. The changes in Ni uptake rates were more pronounced in WH8102 than in CC9311 and for growth on urea or nitrate than for growth on ammonia. These results, combined with an analysis of fully sequenced marine cyanobacterial genomes, suggest that the growth of many marine Synechococcus and all Prochlorococcus strains is dependent upon Ni.

Dupont, CL, Buck KN, Palenik B, Barbeau K.  2010.  Nickel utilization in phytoplankton assemblages from contrasting oceanic regimes. Deep-Sea Research Part I-Oceanographic Research Papers. 57:553-566.   10.1016/j.dsr.2009.12.014   AbstractWebsite

In most oceanic environments, dissolved nickel (Ni) concentrations are drawn clown in surface waters with increasing concentrations at depth, implying a role for biology in the geochemical distribution of Ni Studies with phytoplankton isolates from the surface ocean have established the biochemical roles of Ni in the assimilation of urea and oxidative defense To determine if these requirements are relevant in natural marine planktonic assemblages, bottle-based fertilization experiments were used to test the effects of low-level additions of Ni. urea, or both Ni and urea to surface waters at several locations offshore of Peru and California, as well as in the Gulf of California Urea and Ni(+) urea additions consistently promoted phytoplankton growth relative to control and +Ni treatments, except in a coastal upwelling site and Peruvian water. No effect was observed in the upwelling site, but in Peruvian waters urea additions resulted in increased phytoplankton pigments and phosphate drawdown only when Ni was added concurrently, suggesting a biochemically dependent Ni-urea colimitation In the Gulf of California, Ni additions without urea resulted in increased abundances of cyanobacteria, picoeukaryotes, and the corresponding pigments As urea additions showed the overall phytoplankton community was also urea-limited, it appears that the cyanobactena and potentially the picoeukaryotes were colimited by Ni and urea in a biochemically independent fashion. In parallel, radiotracer-based uptake experiments were used to study the kinetics and spatial variation of biological Ni assimilation. In these experiments, the added radiotracer rarely equilibrated with the natural Ni present, precluding estimates a determination of in situ Ni uptake rates and suggesting that much of the natural Ni was not bioavailable. The lack of equilibration likely did not preclude the measurement of community Ni uptake kinetics, nor the comparison of measured rates between locations The highest V(max)K(p)(-1) values, which reflect a competitive advantage in Ni acquisition at low concentrations, were observed in stratified nitrogen-deplete communities, potentially linking Ni and nitrogen biogeochemistry in a manner consistent with the biochemical utilization of Ni. Overall, uptake rates were higher in the euphotic rather than non-euphotic zone communities, directly reconciling the nutrient-like depth profile of Ni The Ni uptake rates observed at the nitrate-replete Fe-deplete Peru stations were an order of magnitude lower than the other sites This result agrees with calculations suggesting that saturation of the cell surface with Ni and iron (Fe) transporters may limit uptake rates in low Fe waters. (C) 2010 Elsevier Ltd. All rights reserved

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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.