The Unique Biogeochemical Signature of the Marine Diazotroph Trichodesmium

Nuester, Jochen; Vogt, Stefan; Newville, Matthew; Kustka, Adam B.; Twining, Benjamin S.

doi:10.3389/fmicb.2012.00150

Title: The Unique Biogeochemical Signature of the Marine Diazotroph Trichodesmium

Journal Article · Sun Jan 01 00:00:00 EST 2012 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2012.00150· OSTI ID:1628060

Nuester, Jochen ^[1]; Vogt, Stefan ^[2]; Newville, Matthew ^[3]; Kustka, Adam B. ^[4]; Twining, Benjamin S. ^[1]

Bigelow Laboratory for Ocean Sciences, East Boothbay, ME (United States)
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS). X-ray Science Division
Univ. of Chicago, Argonne, IL (United States). Center for Advanced Radiation Sources
Rutgers Univ., Newark, NJ (United States). Dept. of Earth and Environmental Sciences

The elemental composition of phytoplankton can depart from canonical Redfield values under conditions of nutrient limitation or production (e.g., N fixation). Similarly, the trace metal metallome of phytoplankton may be expected to vary as a function of both ambient nutrient concentrations and the biochemical processes of the cell. Diazotrophs such as the colonial cyanobacteria Trichodesmium are likely to have unique metal signatures due to their cell physiology. We present metal (Fe, V, Zn, Ni, Mo, Mn, Cu, Cd) quotas for Trichodesmium collected from the Sargasso Sea which highlight the unique metallome of this organism. The element concentrations of bulk colonies and trichomes sections were analyzed by ICP-MS and synchrotron x-ray fluorescence, respectively. The cells were characterized by low P contents but enrichment in V, Fe, Mo, Ni, and Zn in comparison to other phytoplankton. Vanadium was the most abundant metal in Trichodesmium, and the V quota was up to fourfold higher than the corresponding Fe quota. The stoichiometry of 600C:101N:1P (mol mol-1) reflects P-limiting conditions. Iron and V were enriched in contiguous cells of 10 and 50% of Trichodesmium trichomes, respectively. The distribution of Ni differed from other elements, with the highest concentration in the transverse walls between attached cells. We hypothesize that the enrichments of V, Fe, Mo, and Ni are linked to the biochemical requirements for N fixation either directly through enrichment in the N-fixing enzyme nitrogenase or indirectly by the expression of enzymes responsible for the removal of reactive oxygen species. Unintentional uptake of V via P pathways may also be occurring. Overall, the cellular content of trace metals and macronutrients differs significantly from the (extended) Redfield ratio. TheTrichodesmium metallome is an example of how physiology and environmental conditions can cause significant deviations from the idealized stoichiometry.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1628060

Journal Information:: Frontiers in Microbiology, Vol. 3; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (62)

The Ecology of Arsenic Oremland, Ronald S.; Stolz, John F. ChemInform, Vol. 34, Issue 35 https://doi.org/10.1002/chin.200335257	journal	September 2003
The Chemistry and Biochemistry of Vanadium and the Biological Activities Exerted by Vanadium Compounds Crans, Debbie C.; Smee, Jason J.; Gaidamauskas, Ernestas ChemInform, Vol. 35, Issue 20 https://doi.org/10.1002/chin.200420288	journal	May 2004
Complexation of oxoanions and cationic metals by the biscatecholate siderophore azotochelin Bellenger, Jean-Philippe; Arnaud-Neu, Françoise; Asfari, Zouhair JBIC Journal of Biological Inorganic Chemistry, Vol. 12, Issue 3 https://doi.org/10.1007/s00775-006-0194-6	journal	December 2006
Membrane transport of hydrogen peroxide Bienert, Gerd P.; Schjoerring, Jan K.; Jahn, Thomas P. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 8 https://doi.org/10.1016/j.bbamem.2006.02.015	journal	August 2006
Cellular iron contents of plankton during the Southern Ocean Iron Experiment (SOFeX) Twining, Benjamin S.; Baines, Stephen B.; Fisher, Nicholas S. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 51, Issue 12 https://doi.org/10.1016/j.dsr.2004.08.007	journal	December 2004
Metal quotas of plankton in the equatorial Pacific Ocean Twining, Benjamin S.; Baines, Stephen B.; Bozard, James B. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 58, Issue 3-4 https://doi.org/10.1016/j.dsr2.2010.08.018	journal	February 2011
Influence of anthropogenic combustion emissions on the deposition of soluble aerosol iron to the ocean: Empirical estimates for island sites in the North Atlantic Sholkovitz, Edward R.; Sedwick, Peter N.; Church, Thomas M. Geochimica et Cosmochimica Acta, Vol. 73, Issue 14 https://doi.org/10.1016/j.gca.2009.04.029	journal	July 2009
Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton Tang, Degui; Morel, François M. M. Marine Chemistry, Vol. 98, Issue 1 https://doi.org/10.1016/j.marchem.2005.06.003	journal	January 2006
Uptake and metabolism of arsenate by anexic cultures of the microalgae Dunaliella tertiolecta and Phaeodactylum tricornutum Foster, Simon; Thomson, Danielle; Maher, William Marine Chemistry, Vol. 108, Issue 3-4 https://doi.org/10.1016/j.marchem.2007.11.005	journal	January 2008
Importance of the diazotrophs as a source of new nitrogen in the ocean LaRoche, Julie; Breitbarth, Eike Journal of Sea Research, Vol. 53, Issue 1-2 https://doi.org/10.1016/j.seares.2004.05.005	journal	January 2005
Current status of structure function relationships of vanadium nitrogenase Eady, R. Coordination Chemistry Reviews, Vol. 237, Issue 1-2 https://doi.org/10.1016/s0010-8545(02)00248-5	journal	February 2003
Combined Exposure to Hydrogen Peroxide and LightSelective Effects on Cyanobacteria, Green Algae, and Diatoms Drábková, Michaela; Admiraal, Wim; Maršálek, Blahoslav Environmental Science & Technology, Vol. 41, Issue 1 https://doi.org/10.1021/es060746i	journal	January 2007
Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean Sañudo-Wilhelmy, Sergio A.; Kustka, Adam B.; Gobler, Christopher J. Nature, Vol. 411, Issue 6833 https://doi.org/10.1038/35075041	journal	May 2001
In situ transcriptomic analysis of the globally important keystone N2-fixing taxon Crocosphaera watsonii Hewson, Ian; Poretsky, Rachel S.; Beinart, Roxanne A. The ISME Journal, Vol. 3, Issue 5 https://doi.org/10.1038/ismej.2009.8	journal	February 2009
Decoupling of ammonium regulation and ntcA transcription in the diazotrophic marine cyanobacterium Trichodesmium sp. IMS101 Post, Anton F.; Rihtman, Branko; Wang, Qingfeng The ISME Journal, Vol. 6, Issue 3 https://doi.org/10.1038/ismej.2011.121	journal	September 2011
Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic Mills, Matthew M.; Ridame, Celine; Davey, Margaret Nature, Vol. 429, Issue 6989 https://doi.org/10.1038/nature02550	journal	May 2004
The impact of surface-adsorbed phosphorus on phytoplankton Redfield stoichiometry Sañudo-Wilhelmy, Sergio A.; Tovar-Sanchez, Antonio; Fu, Fei-Xue Nature, Vol. 432, Issue 7019 https://doi.org/10.1038/nature03125	journal	December 2004
Marine microorganisms and global nutrient cycles Arrigo, Kevin R. Nature, Vol. 437, Issue 7057 https://doi.org/10.1038/nature04159	journal	September 2004
Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity Van Mooy, Benjamin A. S.; Fredricks, Helen F.; Pedler, Byron E. Nature, Vol. 458, Issue 7234 https://doi.org/10.1038/nature07659	journal	March 2009
Microbial metalloproteomes are largely uncharacterized Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P. Nature, Vol. 466, Issue 7307 https://doi.org/10.1038/nature09265	journal	July 2010
Dust- and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium Rubin, Maxim; Berman-Frank, Ilana; Shaked, Yeala Nature Geoscience, Vol. 4, Issue 8 https://doi.org/10.1038/ngeo1181	journal	June 2011
Metallomics as integrated biometal science Haraguchi, Hiroki Journal of Analytical Atomic Spectrometry, Vol. 19, Issue 1 https://doi.org/10.1039/b308213j	journal	January 2004
ORGANIZATION OF THEnifGENES OF THE NONHETEROCYSTOUS CYANOBACTERIUMTRICHODESMIUMSP. IMS101 Dominic, Benny; Zani, Sabino; Chen, Yi-Bu Journal of Phycology, Vol. 36, Issue 4 https://doi.org/10.1046/j.1529-8817.2000.99208.x	journal	August 2000
MAPS : A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets Vogt, S. Journal de Physique IV (Proceedings), Vol. 104 https://doi.org/10.1051/jp4:20030160	journal	March 2003
Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry Finzi-Hart, J. A.; Pett-Ridge, J.; Weber, P. K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0810547106	journal	March 2009
Heterologous Expression of the Vanadium-containing Chloroperoxidase from Curvularia inaequalis in Saccharomyces cerevisiae and Site-directed Mutagenesis of the Active Site Residues His496, Lys353, Arg360, and Arg490 Hemrika, Wieger; Renirie, Rokus; Macedo-Ribeiro, Sandra Journal of Biological Chemistry, Vol. 274, Issue 34 https://doi.org/10.1074/jbc.274.34.23820	journal	August 1999
Exploring the Chemistry and Biology of Vanadium-dependent Haloperoxidases Winter, Jaclyn M.; Moore, Bradley S. Journal of Biological Chemistry, Vol. 284, Issue 28 https://doi.org/10.1074/jbc.r109.001602	journal	April 2009
Operational Altimeter Data Processing for Mesoscale Monitoring Leben, Robert R.; Born, George H.; Engebreth, Benjamin R. Marine Geodesy, Vol. 25, Issue 1-2 https://doi.org/10.1080/014904102753516697	journal	February 2002
The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey Sheridan, C. C. Journal of Plankton Research, Vol. 24, Issue 9 https://doi.org/10.1093/plankt/24.9.913	journal	September 2002
The marine cyanobacterium Synechococcus sp. WH7805 requires urease (urea amiohydrolase, EC 3.5.1.5) to utilize urea as a nitrogen source: molecular-genetic and biochemical analysis of the enzyme Collier, Jackie L.; Brahamsha, Bianca; Palenik, Brian Microbiology, Vol. 145, Issue 2 https://doi.org/10.1099/13500872-145-2-447	journal	February 1999
Diazocyte development in the marine diazotrophic cyanobacterium Trichodesmium Sandh, Gustaf; Xu, Linghua; Bergman, Birgitta Microbiology, Vol. 158, Issue 2 https://doi.org/10.1099/mic.0.051268-0	journal	February 2012
Diurnal expression of hetR and diazocyte development in the filamentous non-heterocystous cyanobacterium Trichodesmium erythraeum El-Shehawy, R.; Lugomela, C.; Ernst, A. Microbiology, Vol. 149, Issue 5 https://doi.org/10.1099/mic.0.26170-0	journal	May 2003
Differential phase contrast with a segmented detector in a scanning X-ray microprobe Hornberger, B.; de Jonge, M. D.; Feser, M. Journal of Synchrotron Radiation, Vol. 15, Issue 4 https://doi.org/10.1107/s0909049508008509	journal	May 2008
Quantification of phosphorus in single cells using synchrotron X-ray fluorescence Núñez-Milland, Daliángelis R.; Baines, Stephen B.; Vogt, Stefan Journal of Synchrotron Radiation, Vol. 17, Issue 4 https://doi.org/10.1107/s0909049510014020	journal	May 2010
The Elemental Composition of some Marine Phytoplankton1 Ho, Tung-Yuan; Quigg, Antonietta; Finkel, Zoe V. Journal of Phycology, Vol. 39, Issue 6 https://doi.org/10.1111/j.0022-3646.2003.03-090.x	journal	December 2003
33 Boron in diatoms Deyhle, A.; Hodge, V.; Lewin, R. A. Journal of Phycology, Vol. 39, Issue s1 https://doi.org/10.1111/j.0022-3646.2003.03906001_33.x	journal	June 2003
Primary Structure and Characterization of the Vanadium Chloroperoxidase from the Fungus Curvularia inaequails Simons, Bert H.; Barnett, Philip; Vollenbroek, Esther G. M. European Journal of Biochemistry, Vol. 229, Issue 2 https://doi.org/10.1111/j.1432-1033.1995.tb20499.x	journal	April 1995
Diversity, function and evolution of genes coding for putative Ni-containing superoxide dismutases Dupont, C. L.; Neupane, K.; Shearer, J. Environmental Microbiology, Vol. 10, Issue 7 https://doi.org/10.1111/j.1462-2920.2008.01604.x	journal	July 2008
Essential metals for nitrogen fixation in a free-living N ₂ -fixing bacterium: chelation, homeostasis and high use efficiency : Homeostasis of nitrogenase metal cofactors in Bellenger, J. -P.; Wichard, T.; Xu, Y. Environmental Microbiology, Vol. 13, Issue 6 https://doi.org/10.1111/j.1462-2920.2011.02440.x	journal	March 2011
Acquisition of nitrogen by the shoots of land plants: its occurrence and implications for acid-base regulation Raven, J. A. New Phytologist, Vol. 109, Issue 1 https://doi.org/10.1111/j.1469-8137.1988.tb00212.x	journal	May 1988
The co-evolution of phytoplankton and trace element cycles in the oceans Morel, FranÇOis M. M. Geobiology, Vol. 6, Issue 3 https://doi.org/10.1111/j.1472-4669.2008.00144.x	journal	June 2008
Characterization of a Functional Vanadium-Dependent Bromoperoxidase in the Marine Cyanobacterium Synechococcus sp. Cc93111 Johnson, Todd L.; Palenik, Brian; Brahamsha, Bianca Journal of Phycology, Vol. 47, Issue 4 https://doi.org/10.1111/j.1529-8817.2011.01007.x	journal	June 2011
Cyanobacterial hydrogenases: diversity, regulation and applications Tamagnini, Paula; Leitão, Elsa; Oliveira, Paulo FEMS Microbiology Reviews, Vol. 31, Issue 6 https://doi.org/10.1111/j.1574-6976.2007.00085.x	journal	November 2007
Segregation of Nitrogen Fixation and Oxygenic Photosynthesis in the Marine Cyanobacterium Trichodesmium Berman-Frank, I. Science, Vol. 294, Issue 5546 https://doi.org/10.1126/science.1064082	journal	November 2001
Ni Uptake and Limitation in Marine Synechococcus Strains Dupont, C. L.; Barbeau, K.; Palenik, B. Applied and Environmental Microbiology, Vol. 74, Issue 1 https://doi.org/10.1128/aem.01007-07	journal	October 2007
Nitrogen Fixation and Hydrogen Metabolism in Cyanobacteria Bothe, H.; Schmitz, O.; Yates, M. G. Microbiology and Molecular Biology Reviews, Vol. 74, Issue 4 https://doi.org/10.1128/mmbr.00033-10	journal	November 2010
Hydrogenases and Hydrogen Metabolism of Cyanobacteria Tamagnini, P.; Axelsson, R.; Lindberg, P. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 1 https://doi.org/10.1128/mmbr.66.1.1-20.2002	journal	March 2002
Oxygen relations of nitrogen fixation in cyanobacteria Fay, P. Microbiological Reviews, Vol. 56, Issue 2 https://doi.org/10.1128/mr.56.2.340-373.1992	journal	June 1992
Influence of N substrate on Fe requirements of marine centric diatoms Maldonado, Mt; Price, Nm Marine Ecology Progress Series, Vol. 141 https://doi.org/10.3354/meps141161	journal	January 1996
Colimitation of phytoplankton growth by nickel and nitrogen Price, N. M.; Morel, F. M. M. Limnology and Oceanography, Vol. 36, Issue 6 https://doi.org/10.4319/lo.1991.36.6.1071	journal	September 1991
Interactive influences of bioactive trace metals on biological production in oceanic waters Bruland, Kenneth W.; Donat, John R.; Hutchins, David A. Limnology and Oceanography, Vol. 36, Issue 8 https://doi.org/10.4319/lo.1991.36.8.1555	journal	December 1991
Effect of Zn, Mn, and Fe on Cd accumulation in phytoplankton: Implications for oceanic Cd cycling Sunda, William G.; Huntsman, Susan A. Limnology and Oceanography, Vol. 45, Issue 7 https://doi.org/10.4319/lo.2000.45.7.1501	journal	November 2000
Redfield ratios revisited: Removing the biasing effect of anthropogenic CO₂ Körtzinger, Arne; Hedges, John I.; Quay, Paul D. Limnology and Oceanography, Vol. 46, Issue 4 https://doi.org/10.4319/lo.2001.46.4.0964	journal	June 2001
Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium Berman-Frank, Ilana; Cullen, Jay T.; Shaked, Yeala Limnology and Oceanography, Vol. 46, Issue 6 https://doi.org/10.4319/lo.2001.46.6.1249	journal	August 2001
Iron requirements for dinitrogen- and ammonium-supported growth in cultures of Trichodesmium (IMS 101): Comparison with nitrogen fixation rates and iron: carbon ratios of field populations Kustka, Adam B.; Sañudo-Wilhelmy, Sergio A.; Carpenter, Edward J. Limnology and Oceanography, Vol. 48, Issue 5 https://doi.org/10.4319/lo.2003.48.5.1869	journal	September 2003
Diel variation of molybdenum and iron in marine diazotrophic cyanobacteria Tuit, Caroline; Waterbury, John; Ravizza, Gregory Limnology and Oceanography, Vol. 49, Issue 4 https://doi.org/10.4319/lo.2004.49.4.0978	journal	July 2004
Effects of dust deposition and river discharges on trace metal composition of Trichodesmium spp. in the tropical and subtropical North Atlantic Ocean Tovar-Sanchez, Antonio; Sañudo-Wilhelmy, Sergio A.; Kustka, Adam B. Limnology and Oceanography, Vol. 51, Issue 4 https://doi.org/10.4319/lo.2006.51.4.1755	journal	July 2006
Flexible elemental stoichiometry in Trichodesmium spp. and its ecological implications White, Angelicque E.; Spitz, Yvette H.; Karl, David M. Limnology and Oceanography, Vol. 51, Issue 4 https://doi.org/10.4319/lo.2006.51.4.1777	journal	July 2006
Nitrogen-fixation strategies and Fe requirements in cyanobacteria Berman-Frank, Ilana; Quigg, Antonietta; Finkel, Zoe V. Limnology and Oceanography, Vol. 52, Issue 5 https://doi.org/10.4319/lo.2007.52.5.2260	journal	September 2007
Differential effects of phosphorus limitation on cellular metals in Chlorella and Microcystis Ji, Yongcheng; Sherrell, Robert M. Limnology and Oceanography, Vol. 53, Issue 5 https://doi.org/10.4319/lo.2008.53.5.1790	journal	September 2008
Dissolved inorganic and organic phosphorus uptake in Trichodesmium and the microbial community: The importance of phosphorus ester in the Sargasso Sea Orchard, Elizabeth D.; Ammerman, James W.; Lomas, Michael W. Limnology and Oceanography, Vol. 55, Issue 3 https://doi.org/10.4319/lo.2010.55.3.1390	journal	May 2010
Influence of the Amazon River on dissolved and intra-cellular metal concentrations in <i>Trichodesmium</i> colonies along the western boundary of the sub-tropical North Atlantic Ocean Tovar-Sanchez, A.; Sañudo-Wilhelmy, S. A. Biogeosciences, Vol. 8, Issue 1 https://doi.org/10.5194/bg-8-217-2011	journal	January 2011

Cited By (20)

Limitations on Limitation Laakso, Thomas A.; Schrag, Daniel P. Global Biogeochemical Cycles, Vol. 32, Issue 3 https://doi.org/10.1002/2017gb005832	journal	March 2018
Mineral iron utilization by natural and cultured Trichodesmium and associated bacteria: Mineral Fe utilization by Trichodesmium and bacteria Basu, Subhajit; Shaked, Yeala Limnology and Oceanography, Vol. 63, Issue 6 https://doi.org/10.1002/lno.10939	journal	July 2018
Selective collection of iron-rich dust particles by natural Trichodesmium colonies Kessler, Nivi; Armoza-Zvuloni, Rachel; Wang, Siyuan The ISME Journal, Vol. 14, Issue 1 https://doi.org/10.1038/s41396-019-0505-x	journal	September 2019
Marine nitrogen fixers mediate a low latitude pathway for atmospheric CO2 drawdown Buchanan, Pearse J.; Chase, Zanna; Matear, Richard J. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12549-z	journal	October 2019
Heme in the marine environment: from cells to the iron cycle Hogle, Shane L.; Barbeau, Katherine A.; Gledhill, Martha Metallomics, Vol. 6, Issue 6 https://doi.org/10.1039/c4mt00031e	journal	January 2014
Direct measurement of multi-elements in high matrix samples with a flow injection ICP-MS: application to the extended Emiliania huxleyi Redfield ratio Zhang, Qiong; Snow, Joseph T.; Holdship, Phil Journal of Analytical Atomic Spectrometry, Vol. 33, Issue 7 https://doi.org/10.1039/c8ja00031j	journal	January 2018
Primary productivity induced by iron and nitrogen in the Tasman Sea: an overview of the PINTS expedition Hassler, C. S.; Ridgway, K. R.; Bowie, A. R. Marine and Freshwater Research, Vol. 65, Issue 6 https://doi.org/10.1071/mf13137	journal	January 2014
Climate-driven oscillation of phosphorus and iron limitation in the North Pacific Subtropical Gyre Letelier, Ricardo M.; Björkman, Karin M.; Church, Matthew J. Proceedings of the National Academy of Sciences, Vol. 116, Issue 26 https://doi.org/10.1073/pnas.1900789116	journal	June 2019
Trace Metal Imaging of Sulfate-Reducing Bacteria and Methanogenic Archaea at Single-Cell Resolution by Synchrotron X-Ray Fluorescence Imaging Glass, Jennifer B.; Chen, Si; Dawson, Katherine S. Geomicrobiology Journal, Vol. 35, Issue 1 https://doi.org/10.1080/01490451.2017.1321068	journal	May 2017
Evidence for polyploidy in the globally important diazotroph Trichodesmium Sargent, Elizabeth C.; Hitchcock, Andrew; Johansson, S. Andreas FEMS Microbiology Letters, Vol. 363, Issue 21 https://doi.org/10.1093/femsle/fnw244	journal	October 2016
Effects of Trace Metal Concentrations on the Growth of the Coral Endosymbiont Symbiodinium kawagutii Rodriguez, Irene B.; Lin, Senjie; Ho, Jiaxuan Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00082	journal	February 2016
Impacts of Aerosol Copper on Marine Phytoplankton: A Review Yang, Tianjiao; Chen, Ying; Zhou, Shengqian Atmosphere, Vol. 10, Issue 7 https://doi.org/10.3390/atmos10070414	journal	July 2019
Limitations on Limitation Laakso, Thomas A.; Schrag, Daniel P. GSA Annual Meeting in Seattle, Washington, USA - 2017, Geological Society of America Abstracts with Programs https://doi.org/10.1130/abs/2017am-306231	conference	January 2017
Trace Metal Imaging of Sulfate-Reducing Bacteria and Methanogenic Archaea at Single-Cell Resolution by Synchrotron X-Ray Fluorescence Imaging [Supplemental Data] Glass, Jennifer; Chen, Si; Dawson, Katherine figshare-Supplementary information for journal article at DOI: 10.1080/01490451.2017.1321068, 1 PDF file (837.71 kB) https://doi.org/10.6084/m9.figshare.4900607	dataset	May 2017
Trace metal imaging of sulfate-reducing bacteria and methanogenic archaea at single-cell resolution by synchrotron X-ray fluorescence imaging [Supplemental Data] Glass, Jennifer; Chen, Si; Dawson, Katherine figshare-Supplementary information for journal article at DOI: 10.1080/01490451.2017.1321068, 1 PDF file (837.71 kB) https://doi.org/10.6084/m9.figshare.4900607.v1	dataset	April 2017
Quantifying Integrated Proteomic Responses to Iron Stress in the Globally Important Marine Diazotroph Trichodesmium Snow, Joseph T.; Polyviou, Despo; Skipp, Paul PLOS ONE, Vol. 10, Issue 11 https://doi.org/10.1371/journal.pone.0142626	journal	November 2015
Biogeochemical cycle of iron : distribution and speciation in the North Atlantic Ocean (GA01) and the Southern Ocean (GIpr05) (GEOTRACES) Tonnard, M. University of Tasmania https://doi.org/10.25959/100.00031961	text	January 2019
Molybdenum limitation of microbial nitrogen assimilation in aquatic ecosystems and pure cultures Glass, Jennifer B.; Axler, Richard P.; Chandra, Sudeep Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00331	journal	January 2012
Regression modeling of the North East Atlantic Spring Bloom suggests previously unrecognized biological roles for V and Mo Klein, Nick J.; Beck, A. J.; Hutchins, D. A. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00045	journal	January 2013
The environmental bioinorganic chemistry of aquatic microbial organisms Gledhill, Martha; Hassler, Christel S.; Schoemann, Veronique Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00100	journal	January 2013

Similar Records

Mechanisms and heterogeneity of in situ mineral processing by the marine nitrogen fixer Trichodesmium revealed by single-colony metaproteomics

Journal Article · Tue Jul 13 00:00:00 EDT 2021 · ISME Communications · OSTI ID:1628060

Held, Noelle A.; Sutherland, Kevin M.; Webb, Eric A.; +7 more

A nutrient limitation mosaic in the eastern tropical Indian Ocean

Journal Article · Fri May 17 00:00:00 EDT 2019 · Deep-Sea Research. Part 2. Topical Studies in Oceanography · OSTI ID:1628060

Twining, Benjamin S.; Rauschenberg, Sara; Baer, Steven E.; +3 more

Selective collection of iron-rich dust particles by natural Trichodesmium colonies

Journal Article · Tue Sep 24 00:00:00 EDT 2019 · The ISME Journal · OSTI ID:1628060

Kessler, Nivi; Armoza-Zvuloni, Rachel; Wang, Siyuan; +4 more

Related Subjects

54 ENVIRONMENTAL SCIENCES
59 BASIC BIOLOGICAL SCIENCES
Microbiology
extended redfield ratio
metallome
nitrogen fixation
vanadium
iron
nickel
zinc

Title: The Unique Biogeochemical Signature of the Marine Diazotroph Trichodesmium

Citation Formats

References (62)

Cited By (20)

Similar Records

Related Subjects