Widner
Brittany
Widner
Brittany
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ArticleHigh rates of N-2 fixation in temperate, western North Atlantic coastal waters expand the realm of marine diazotrophy(American Geophysical Union, 2019-06-10) Mulholland, Margaret R. ; Bernhardt, Peter W. ; Widner, Brittany ; Selden, Corday ; Chappell, Phoebe Dreux ; Clayton, Sophie A. ; Mannino, Antonio ; Hyde, Kimberly J. W.Dinitrogen (N2) fixation can alleviate N limitation of primary productivity by introducing fixed nitrogen (N) to the world's oceans. Although measurements of pelagic marine N2 fixation are predominantly from oligotrophic oceanic regions, where N limitation is thought to favor growth of diazotrophic microbes, here we report high rates of N2 fixation from seven cruises spanning four seasons in temperate, western North Atlantic coastal waters along the North American continental shelf between Cape Hatteras and Nova Scotia, an area representing 6.4% of the North Atlantic continental shelf area. Integrating average areal rates of N2 fixation during each season and for each domain in the study area, the estimated N input from N2 fixation to this temperate shelf system is 0.02 Tmol N/year, an amount equivalent to that previously estimated for the entire North Atlantic continental shelf. Unicellular group A cyanobacteria (UCYN‐A) were most often the dominant diazotrophic group expressing nifH, a gene encoding the nitrogenase enzyme, throughout the study area during all seasons. This expands the domain of these diazotrophs to include coastal waters where dissolved N concentrations are not always depleted. Further, the high rates of N2 fixation and diazotroph diversity along the western North Atlantic continental shelf underscore the need to reexamine the biogeography and the activity of diazotrophs along continental margins. Accounting for this substantial but previously overlooked source of new N to marine systems necessitates revisions to global marine N budgets.
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ArticlePotential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters(Springer Nature, 2020-11-16) Gazitúa, M. Consuelo ; Vik, Dean R. ; Roux, Simon ; Gregory, Ann C. ; Bolduc, Benjamin ; Widner, Brittany ; Mulholland, Margaret R. ; Hallam, Steven J. ; Ulloa, Osvaldo ; Sullivan, Matthew B.Viruses play an important role in the ecology and biogeochemistry of marine ecosystems. Beyond mortality and gene transfer, viruses can reprogram microbial metabolism during infection by expressing auxiliary metabolic genes (AMGs) involved in photosynthesis, central carbon metabolism, and nutrient cycling. While previous studies have focused on AMG diversity in the sunlit and dark ocean, less is known about the role of viruses in shaping metabolic networks along redox gradients associated with marine oxygen minimum zones (OMZs). Here, we analyzed relatively quantitative viral metagenomic datasets that profiled the oxygen gradient across Eastern Tropical South Pacific (ETSP) OMZ waters, assessing whether OMZ viruses might impact nitrogen (N) cycling via AMGs. Identified viral genomes encoded six N-cycle AMGs associated with denitrification, nitrification, assimilatory nitrate reduction, and nitrite transport. The majority of these AMGs (80%) were identified in T4-like Myoviridae phages, predicted to infect Cyanobacteria and Proteobacteria, or in unclassified archaeal viruses predicted to infect Thaumarchaeota. Four AMGs were exclusive to anoxic waters and had distributions that paralleled homologous microbial genes. Together, these findings suggest viruses modulate N-cycling processes within the ETSP OMZ and may contribute to nitrogen loss throughout the global oceans thus providing a baseline for their inclusion in the ecosystem and geochemical models.
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ArticleToward resolving disparate accounts of the extent and magnitude of nitrogen fixation in the Eastern Tropical South Pacific oxygen deficient zone(Association for the Sciences of Limnology and Oceanography, 2021-04-07) Selden, Corday ; Mulholland, Margaret R. ; Widner, Brittany ; Bernhardt, Peter W. ; Jayakumar, AmalExamination of dinitrogen (N2) fixation in the Eastern Tropical South Pacific oxygen deficient zone has raised questions about the range of diazotrophs in the deep sea and their quantitative importance as a source of new nitrogen globally. However, technical considerations in the deployment of stable isotopes in quantifying N2 fixation rates have complicated interpretation of this research. Here, we report the findings of a comprehensive survey of N2 fixation within, above and below the Eastern Tropical South Pacific oxygen deficient zone. N2 fixation rates were measured using a robust 15N tracer method (bubble removal) that accounts for the slow dissolution of N2 gas and calculated using a conservative approach. N2 fixation was only detected in a subset of samples (8 of 125 replicated measurements) collected within suboxic waters (< 20 μmol O2 kg−1) or at the oxycline. Most of these detectable rates were measured at nearshore stations, or where surface productivity was high. These findings support the hypothesis that low oxygen/high organic carbon conditions favor non-cyanobacterial diazotrophs. Nevertheless, this study indicates that N2 fixation is neither widespread nor quantitatively important throughout this region.
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ArticleQuantification of amine- and alcohol-containing metabolites in saline samples using pre-extraction benzoyl chloride derivatization and ultrahigh performance liquid chromatography tandem mass spectrometry (UHPLC MS/MS)(American Chemical Society, 2021-03-10) Widner, Brittany ; Kido Soule, Melissa C. ; Ferrer-González, Frank Xavier ; Moran, Mary Ann ; Kujawinski, Elizabeth B.Dissolved metabolites serve as nutrition, energy, and chemical signals for microbial systems. However, the full scope and magnitude of these processes in marine systems are unknown, largely due to insufficient methods, including poor extraction of small, polar compounds using common solid-phase extraction resins. Here, we utilized pre-extraction derivatization and ultrahigh performance liquid chromatography electrospray ionization tandem mass spectrometry (UHPLC-ESI-MS/MS) to detect and quantify targeted dissolved metabolites in seawater and saline culture media. Metabolites were derivatized with benzoyl chloride by their primary and secondary amine and alcohol functionalities and quantified using stable isotope-labeled internal standards (SIL-ISs) produced from 13C6-labeled benzoyl chloride. We optimized derivatization, extraction, and sample preparation for field and culture samples and evaluated matrix-derived biases. We have optimized this quantitative method for 73 common metabolites, of which 50 cannot be quantified without derivatization due to low extraction efficiencies. Of the 73 metabolites, 66 were identified in either culture media or seawater and 45 of those were quantified. This derivatization method is sensitive (detection limits = pM to nM), rapid (∼5 min per sample), and high throughput.
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ArticleAssessing phytoplankton nutritional status and potential impact of wet deposition in seasonally oligotrophic waters of the Mid‐Atlantic Bight(John Wiley & Sons, 2018-04-06) Sedwick, Peter N. ; Bernhardt, Peter W. ; Mulholland, Margaret R. ; Najjar, Raymond G. ; Blumen, L. M. ; Sohst, Bettina M. ; Sookhdeo, C. ; Widner, BrittanyTo assess phytoplankton nutritional status in seasonally oligotrophic waters of the southern Mid‐Atlantic Bight, and the potential for rain to stimulate primary production in this region during summer, shipboard bioassay experiments were performed using natural seawater and phytoplankton collected north and south of the Gulf Stream. Bioassay treatments comprised iron, nitrate, iron + nitrate, iron + nitrate + phosphate, and rainwater. Phytoplankton growth was inferred from changes in chlorophyll a, inorganic nitrogen, and carbon‐13 uptake, relative to unamended control treatments. Results indicated the greatest growth stimulation by iron + nitrate + phosphate, intermediate growth stimulation by rainwater, modest growth stimulation by nitrate and iron + nitrate, and no growth stimulation by iron. Based on these data and analysis of seawater and atmospheric samples, nitrogen was the proximate limiting nutrient, with a secondary limitation imposed by phosphorus. Our results imply that summer rain events increase new production in these waters by contributing nitrogen and phosphorus, with the availability of the latter setting the upper limit on rain‐stimulated new production.
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ArticleDinitrogen fixation across physico-chemical gradients of the Eastern Tropical North Pacific oxygen deficient zone(American Geophysical Union, 2019-09-04) Selden, Corday ; Mulholland, Margaret R. ; Bernhardt, Peter W. ; Widner, Brittany ; Macias-Tapia, Alfonso ; Ji, Qixing ; Jayakumar, D. A.The Eastern Tropical North Pacific Ocean hosts one of the world's largest oceanic oxygen deficient zones (ODZs). Hot spots for reactive nitrogen (Nr) removal processes, ODZs generate conditions proposed to promote Nr inputs via dinitrogen (N2) fixation. In this study, we quantified N2 fixation rates by 15N tracer bioassay across oxygen, nutrient, and light gradients within and adjacent to the ODZ. Within subeuphotic oxygen‐deplete waters, N2 fixation was largely undetectable; however, addition of dissolved organic carbon stimulated N2 fixation in suboxic (<20 μmol/kg O2) waters, suggesting that diazotroph communities are likely energy limited or carbon limited and able to fix N2 despite high ambient concentrations of dissolved inorganic nitrogen. Elevated rates (>9 nmol N·L−1·day−1) were also observed in suboxic waters near volcanic islands where N2 fixation was quantifiable to 3,000 m. Within the overlying euphotic waters, N2 fixation rates were highest near the continent, exceeding 500 μmol N·m−2·day−1 at one third of inshore stations. These findings support the expansion of the known range of diazotrophs to deep, cold, and dissolved inorganic nitrogen‐replete waters. Additionally, this work bolsters calls for the reconsideration of ocean margins as important sources of Nr. Despite high rates at some inshore stations, regional N2 fixation appears insufficient to compensate for Nr loss locally as observed previously in the Eastern Tropical South Pacific ODZ.
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ArticleResource partitioning of phytoplankton metabolites that support bacterial heterotrophy(Springer Nature, 2020-10-23) Ferrer-González, Frank Xavier ; Widner, Brittany ; Holderman, Nicole R. ; Glushka, John ; Edison, Arthur S. ; Kujawinski, Elizabeth B. ; Moran, Mary AnnThe communities of bacteria that assemble around marine microphytoplankton are predictably dominated by Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. Yet whether this consistent ecological pattern reflects the result of resource-based niche partitioning or resource competition requires better knowledge of the metabolites linking microbial autotrophs and heterotrophs in the surface ocean. We characterized molecules targeted for uptake by three heterotrophic bacteria individually co-cultured with a marine diatom using two strategies that vetted the exometabolite pool for biological relevance by means of bacterial activity assays: expression of diagnostic genes and net drawdown of exometabolites, the latter detected with mass spectrometry and nuclear magnetic resonance using novel sample preparation approaches. Of the more than 36 organic molecules with evidence of bacterial uptake, 53% contained nitrogen (including nucleosides and amino acids), 11% were organic sulfur compounds (including dihydroxypropanesulfonate and dimethysulfoniopropionate), and 28% were components of polysaccharides (including chrysolaminarin, chitin, and alginate). Overlap in phytoplankton-derived metabolite use by bacteria in the absence of competition was low, and only guanosine, proline, and N-acetyl-d-glucosamine were predicted to be used by all three. Exometabolite uptake pattern points to a key role for ecological resource partitioning in the assembly marine bacterial communities transforming recent photosynthate.
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ArticleMigratory zooplankton excreta and its influence on prokaryotic communities(Frontiers Media, 2020-12-01) Maas, Amy E. ; Liu, Shuting ; Bolaños, Luis M. ; Widner, Brittany ; Parsons, Rachel ; Kujawinski, Elizabeth B. ; Blanco-Bercial, Leocadio ; Carlson, Craig A.Particulate organic matter (POM) (fecal pellets) from zooplankton has been demonstrated to be an important nutrient source for the pelagic prokaryotic community. Significantly less is known about the chemical composition of the dissolved organic matter (DOM) produced by these eukaryotes and its influence on pelagic ecosystem structure. Zooplankton migrators, which daily transport surface-derived compounds to depth, may act as important vectors of limiting nutrients for mesopelagic microbial communities. In this role, zooplankton may increase the DOM remineralization rate by heterotrophic prokaryotes through the creation of nutrient rich “hot spots” that could potentially increase niche diversity. To explore these interactions, we collected the migratory copepod Pleuromamma xiphias from the northwestern Sargasso Sea and sampled its excreta after 12–16 h of incubation. We measured bulk dissolved organic carbon (DOC), dissolved free amino acids (DFAA) via high performance liquid chromatography and dissolved targeted metabolites via quantitative mass spectrometry (UPLC-ESI-MSMS) to quantify organic zooplankton excreta production and characterize its composition. We observed production of labile DOM, including amino acids, vitamins, and nucleosides. Additionally, we harvested a portion of the excreta and subsequently used it as the growth medium for mesopelagic (200 m) bacterioplankton dilution cultures. In zooplankton excreta treatments we observed a four-fold increase in bacterioplankton cell densities that reached stationary growth phase after five days of dark incubation. Analyses of 16S rRNA gene amplicons suggested a shift from oligotrophs typical of open ocean and mesopelagic prokaryotic communities to more copiotrophic bacterial lineages in the presence of zooplankton excreta. These results support the hypothesis that zooplankton and prokaryotes are engaged in complex and indirect ecological interactions, broadening our understanding of the microbial loop.
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ArticleSeasonal and daily patterns in known dissolved metabolites in the northwestern Sargasso Sea(Association for the Sciences of Limnology and Oceanography, 2024-01-10) Longnecker, Krista ; Kido Soule, Melissa C. ; Swarr, Gretchen J. ; Parsons, Rachel J. ; Liu, Shuting ; Johnson, Winifred M. ; Widner, Brittany ; Curry, Ruth G. ; Carlson, Craig A. ; Kujawinski, Elizabeth B.Organic carbon in seawater plays a significant role in the global carbon cycle. The concentration and composition of dissolved organic carbon reflect the activity of the biological community and chemical reactions that occur in seawater. From 2016 to 2019, we repeatedly sampled the oligotrophic northwest Sargasso Sea in the vicinity of the Bermuda Atlantic Time-series Study site (BATS) to quantitatively follow known compounds within the pool of dissolved organic matter in the upper 1000 m of the water column. Most metabolites showed surface enrichment, and 83% of the metabolites had significantly lower concentrations with increasing depth. Dissolved metabolite concentrations most notably revealed temporal variability. Fourteen metabolites displayed seasonality that was repeated in each of the 4 yr sampled. Concentrations of vitamins, including pantothenic acid (vitamin B5) and riboflavin (vitamin B2), increased annually during winter periods when mixed layer depths were deepest. During diel sampling, light-sensitive riboflavin decreased significantly during daylight hours. The temporal variability in metabolites at BATS was less than the spatial variability in metabolites from a previous sample set collected over a broad latitudinal range in the western Atlantic Ocean. The metabolites examined in this study are all components of central carbon metabolism. By examining these metabolites at finer resolution and in a time-series, we begin to provide insights into the chemical compounds that may be exchanged by microorganisms in marine systems, data which are fundamental to understanding the chemical response of marine systems to future changes in climate.