Patterns of iron and siderophore distributions across the California Current System

Boiteau, Rene M.; Till, Claire P.; Coale, Tyler H.; Fitzsimmons, Jessica N.; Bruland, Kenneth W.; Repeta, Daniel J.

doi:10.1002/lno.11046

Title: Patterns of iron and siderophore distributions across the California Current System

Journal Article · 08 November 2018 · Limnology and Oceanography

DOI: https://doi.org/10.1002/lno.11046 · OSTI ID:1507753

^[1];

^[2]; Coale, Tyler H. ^[3];

^[4]; Bruland, Kenneth W. ^[5]; Repeta, Daniel J. ^[6]

Woods Hole Oceanographic Inst., MA (United States). Dept. of Marine Chemistry and Geochemistry; Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Earth, Atmospheric, and Planetary Sciences; Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.
Univ. of California, Santa Cruz, CA (United States). Ocean Sciences Dept.; Humboldt State Univ., Arcata, CA (United States). Chemistry Dept.
Univ. of California, San Diego, CA (United States). Scripps Inst. of Oceanography
Texas A & M Univ., College Station, TX (United States). Dept. of Oceanography; Rutgers Univ., New Brunswick, NJ (United States). Dept. of Marine & Coastal Sciences
Univ. of California, Santa Cruz, CA (United States). Ocean Sciences Dept.
Woods Hole Oceanographic Inst., MA (United States). Dept. of Marine Chemistry and Geochemistry

Coastal upwelling of nutrients and metals along eastern boundary currents fuels some of the most biologically productive marine ecosystems. Although iron is a main driver of productivity in many of these regions, iron cycling and acquisition by microbes remain poorly constrained, in part due to the unknown composition of organic ligands that keep bioavailable iron in solution. We investigated organic ligand composition in discrete water samples collected across the highly productive California Coastal upwelling system. Siderophores were observed in distinct nutrient regimes at concentrations ranging from 1 pM to 18 pM. Near the shallow continental shelf, ferrioxamine B was observed in recently upwelled, high chlorophyll surface waters while synechobactins were identified within nepheloid layers at 60–90 m depth. In offshore waters characterized by intermediate chlorophyll, iron, and nitrate concentrations, we found amphibactins and an unknown siderophore with a molecular formula of C₃₃H₅₈O₈N₅Fe. Highest concentrations were measured in the photic zone, however, amphibactins were also found in waters as deep as 1500 m. The distribution of siderophores provides evidence for microbial iron deficiency across a range of nutrient regimes and indicates siderophore production and acquisition is an important strategy for biological iron uptake in iron limited coastal systems. Polydisperse humic ligands were also detected throughout the water column and were particularly abundant near the benthic boundary. Our results highlight the fine-scale spatial heterogeneity of metal ligand composition in an upwelling environment and elucidate distinct sources that include biological production and the degradation of organic matter in suboxic waters.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Univ. of California, Santa Cruz, CA (United States); Woods Hole Oceanographic Inst., MA (United States)

Sponsoring Organization:: Gordon and Betty Moore Foundation (United States); National Science Foundation (NSF) (United States); PNNL Laboratory Directed Research and Development (LDRD) Program; Simons Foundation (United States); USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1507753

Report Number(s):: PNNL-SA-138032

Journal Information:: Limnology and Oceanography, Journal Name: Limnology and Oceanography Journal Issue: 1 Vol. 64; ISSN 0024-3590

Publisher:: Association for the Sciences of Limnology and Oceanography - WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (61)

Scandium in the open ocean: A comparison with other group 3 trivalent metals Parker, C. E.; Brown, M. T.; Bruland, K. W. Geophysical Research Letters, Vol. 43, Issue 6 https://doi.org/10.1002/2016GL067827	journal	March 2016
Crochelins: Siderophores with an Unprecedented Iron-Chelating Moiety from the Nitrogen-Fixing Bacterium Azotobacter chroococcum Baars, Oliver; Zhang, Xinning; Gibson, Marcus I. Angewandte Chemie, Vol. 130, Issue 2 https://doi.org/10.1002/ange.201709720	journal	December 2017
Crochelins: Siderophores with an Unprecedented Iron-Chelating Moiety from the Nitrogen-Fixing Bacterium Azotobacter chroococcum Baars, Oliver; Zhang, Xinning; Gibson, Marcus I. Angewandte Chemie International Edition, Vol. 57, Issue 2 https://doi.org/10.1002/anie.201709720	journal	December 2017
Mineralization of dissolved organic carbon in the Sargasso Sea Hansell, Dennis A.; Bates, Nicholas R.; Gundersen, Kjell Marine Chemistry, Vol. 51, Issue 3 https://doi.org/10.1016/0304-4203(95)00063-1	journal	December 1995
The heat shock response of the cryptobiotic brine shrimp Artemia — II. Heat shock proteins Miller, David; McLennan, Alexander G. Journal of Thermal Biology, Vol. 13, Issue 3 https://doi.org/10.1016/0306-4565(88)90023-X	journal	July 1988
Sampling and analytical methods for the determination of copper, cadmium, zinc, and nickel at the nanogram per liter level in sea water Bruland, Kenneth W.; Franks, Robert P.; Knauer, George A. Analytica Chimica Acta, Vol. 105 https://doi.org/10.1016/S0003-2670(01)83754-5	journal	March 1979
Fluxes of dissolved organic carbon from California continental margin sediments Burdige, David J.; Berelson, William M.; Coale, Kenneth H. Geochimica et Cosmochimica Acta, Vol. 63, Issue 10 https://doi.org/10.1016/S0016-7037(99)00066-6	journal	May 1999
Suspended sediment transport on the continental shelf near Davenport, California Xu, J. P.; Noble, Marlene; Eittreim, Stephen L. Marine Geology, Vol. 181, Issue 1-3 https://doi.org/10.1016/S0025-3227(01)00266-3	journal	March 2002
A time series of benthic flux measurements from Monterey Bay, CA Berelson, William; McManus, Jim; Coale, Kenneth Continental Shelf Research, Vol. 23, Issue 5 https://doi.org/10.1016/S0278-4343(03)00009-8	journal	March 2003
Collection and detection of natural iron-binding ligands from seawater Macrellis, Heather M.; Trick, Charles G.; Rue, Eden L. Marine Chemistry, Vol. 76, Issue 3 https://doi.org/10.1016/S0304-4203(01)00061-5	journal	November 2001
Coastal iron and nitrate distributions during the spring and summer upwelling season in the central California Current upwelling regime Biller, Dondra V.; Coale, Tyler H.; Till, Ralph C. Continental Shelf Research, Vol. 66 https://doi.org/10.1016/j.csr.2013.07.003	journal	September 2013
The flux of iron and iron isotopes from San Pedro Basin sediments John, Seth G.; Mendez, Jeffery; Moffett, James Geochimica et Cosmochimica Acta, Vol. 93 https://doi.org/10.1016/j.gca.2012.06.003	journal	September 2012
Modeling studies of dissolved organic matter cycling in Santa Barbara Basin (CA, USA) sediments Burdige, David J.; Komada, Tomoko; Magen, Cédric Geochimica et Cosmochimica Acta, Vol. 195 https://doi.org/10.1016/j.gca.2016.09.007	journal	December 2016
Production of siderophore type chelates by mixed bacterioplankton populations in nutrient enriched seawater incubations Gledhill, Martha; McCormack, Paul; Ussher, Simon Marine Chemistry, Vol. 88, Issue 1-2 https://doi.org/10.1016/j.marchem.2004.03.003	journal	August 2004
Iron, macronutrients and diatom blooms in the Peru upwelling regime: brown and blue waters of Peru Bruland, Kenneth W.; Rue, Eden L.; Smith, Geoffrey J. Marine Chemistry, Vol. 93, Issue 2-4 https://doi.org/10.1016/j.marchem.2004.06.011	journal	January 2005
Production of siderophore type chelates in Atlantic Ocean waters enriched with different carbon and nitrogen sources Mawji, Edward; Gledhill, Martha; Milton, James A. Marine Chemistry, Vol. 124, Issue 1-4 https://doi.org/10.1016/j.marchem.2010.12.005	journal	March 2011
Analysis of Mn, Fe, Co, Ni, Cu, Zn, Cd, and Pb in seawater using the Nobias-chelate PA1 resin and magnetic sector inductively coupled plasma mass spectrometry (ICP-MS) Biller, Dondra V.; Bruland, Kenneth W. Marine Chemistry, Vol. 130-131 https://doi.org/10.1016/j.marchem.2011.12.001	journal	February 2012
Sources and distributions of Mn, Fe, Co, Ni, Cu, Zn, and Cd relative to macronutrients along the central California coast during the spring and summer upwelling season Biller, Dondra V.; Bruland, Kenneth W. Marine Chemistry, Vol. 155 https://doi.org/10.1016/j.marchem.2013.06.003	journal	September 2013
Iron-binding ligands and humic substances in the San Francisco Bay estuary and estuarine-influenced shelf regions of coastal California Bundy, Randelle M.; Abdulla, Hussain A. N.; Hatcher, Patrick G. Marine Chemistry, Vol. 173 https://doi.org/10.1016/j.marchem.2014.11.005	journal	July 2015
Organic speciation of dissolved iron in estuarine and coastal waters at multiple analytical windows Mahmood, Abida; Abualhaija, Mahmoud M.; van den Berg, Constant M. G. Marine Chemistry, Vol. 177 https://doi.org/10.1016/j.marchem.2015.11.001	journal	December 2015
Patterns and processes in the California Current System Checkley, David M.; Barth, John A. Progress in Oceanography, Vol. 83, Issue 1-4 https://doi.org/10.1016/j.pocean.2009.07.028	journal	December 2009
The central California Current transition zone: A broad region exhibiting evidence for iron limitation Biller, Dondra V.; Bruland, Kenneth W. Progress in Oceanography, Vol. 120 https://doi.org/10.1016/j.pocean.2013.11.002	journal	January 2014
Detection of Iron Ligands in Seawater and Marine Cyanobacteria Cultures by High-Performance Liquid Chromatography–Inductively Coupled Plasma-Mass Spectrometry Boiteau, Rene M.; Fitzsimmons, Jessica N.; Repeta, Daniel J. Analytical Chemistry, Vol. 85, Issue 9 https://doi.org/10.1021/ac3034568	journal	April 2013
ChelomEx: Isotope-Assisted Discovery of Metal Chelates in Complex Media Using High-Resolution LC-MS Baars, Oliver; Morel, François M. M.; Perlman, David H. Analytical Chemistry, Vol. 86, Issue 22 https://doi.org/10.1021/ac503000e	journal	October 2014
Microbial Iron Acquisition: Marine and Terrestrial Siderophores Sandy, Moriah; Butler, Alison Chemical Reviews, Vol. 109, Issue 10 https://doi.org/10.1021/cr9002787	journal	October 2009
Hydroxamate Siderophores: Occurrence and Importance in the Atlantic Ocean Mawji, Edward; Gledhill, Martha; Milton, James A. Environmental Science & Technology, Vol. 42, Issue 23 https://doi.org/10.1021/es801884r	journal	December 2008
The flux of iron from continental shelf sediments: A missing source for global budgets: FLUX OF IRON FROM THE CONTINENTAL SHELF Elrod, Virginia A.; Berelson, William M.; Coale, Kenneth H. Geophysical Research Letters, Vol. 31, Issue 12 https://doi.org/10.1029/2004GL020216	journal	June 2004
A long-term, high-resolution record of surface water iron concentrations in the upwelling-driven central California region Elrod, V. A.; Johnson, K. S.; Fitzwater, S. E. Journal of Geophysical Research, Vol. 113, Issue C11 https://doi.org/10.1029/2007JC004610	journal	January 2008
Factors influencing the chemistry of the near-field Columbia River plume: Nitrate, silicic acid, dissolved Fe, and dissolved Mn Bruland, Kenneth W.; Lohan, Maeve C.; Aguilar-Islas, Ana M. Journal of Geophysical Research, Vol. 113 https://doi.org/10.1029/2007JC004702	journal	January 2008
Dissolved iron and macronutrient distributions in the southern California Current System King, Andrew L.; Barbeau, Katherine A. Journal of Geophysical Research, Vol. 116, Issue C3 https://doi.org/10.1029/2010JC006324	journal	January 2011
The large-scale summer circulation of the California Current Strub, P. Ted; James, Corinne Geophysical Research Letters, Vol. 22, Issue 3 https://doi.org/10.1029/94GL03011	journal	February 1995
The California Current system: The seasonal variability of its physical characteristics Lynn, Ronald J.; Simpson, James J. Journal of Geophysical Research, Vol. 92, Issue C12 https://doi.org/10.1029/JC092iC12p12947	journal	January 1987
Continental-shelf sediment as a primary source of iron for coastal phytoplankton Johnson, Kenneth S.; Chavez, Francisco P.; Friederich, Gernot E. Nature, Vol. 398, Issue 6729 https://doi.org/10.1038/19511	journal	April 1999
A cross-platform toolkit for mass spectrometry and proteomics Chambers, Matthew C.; Maclean, Brendan; Burke, Robert Nature Biotechnology, Vol. 30, Issue 10 https://doi.org/10.1038/nbt.2377	journal	October 2012
Microbial biogeochemistry of coastal upwelling regimes in a changing ocean Capone, Douglas G.; Hutchins, David A. Nature Geoscience, Vol. 6, Issue 9 https://doi.org/10.1038/ngeo1916	journal	August 2013
Metallophore mapping in complex matrices by metal isotope coded profiling of organic ligands Deicke, Michael; Mohr, Jan Frieder; Bellenger, Jean-Philippe The Analyst, Vol. 139, Issue 23 https://doi.org/10.1039/C4AN01461H	journal	January 2014
Amphiphilic siderophore production by oil-associating microbes Kem, Michelle P.; Zane, Hannah K.; Springer, Stephen D. Metallomics, Vol. 6, Issue 6 https://doi.org/10.1039/C4MT00047A	journal	January 2014
An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS Boiteau, Rene M.; Repeta, Daniel J. Metallomics, Vol. 7, Issue 5 https://doi.org/10.1039/C5MT00005J	journal	January 2015
Chemistry and biology of siderophores Hider, Robert C.; Kong, Xiaole Natural Product Reports, Vol. 27, Issue 5 https://doi.org/10.1039/b906679a	journal	January 2010
Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium Martinez, J. S.; Carter-Franklin, J. N.; Mann, E. L. Proceedings of the National Academy of Sciences, Vol. 100, Issue 7 https://doi.org/10.1073/pnas.0637444100	journal	March 2003
Influence of ocean winds on the pelagic ecosystem in upwelling regions Rykaczewski, R. R.; Checkley, D. M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 6 https://doi.org/10.1073/pnas.0711777105	journal	February 2008
Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean Boiteau, Rene M.; Mende, Daniel R.; Hawco, Nicholas J. Proceedings of the National Academy of Sciences, Vol. 113, Issue 50 https://doi.org/10.1073/pnas.1608594113	journal	December 2016
PubChem Substance and Compound databases Kim, Sunghwan; Thiessen, Paul A.; Bolton, Evan E. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv951	journal	September 2015
Iron transporters in marine prokaryotic genomes and metagenomes: Iron transporters in marine prokaryotes Hopkinson, Brian M.; Barbeau, Katherine A. Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2011.02539.x	journal	August 2011
Transcriptional regulation of the desferrioxamine gene cluster of Streptomyces coelicolor is mediated by binding of DmdR1 to an iron box in the promoter of the desA gene : Regulation of the desferrioxamine gene cluster Tunca, Sedef; Barreiro, Carlos; Sola-Landa, Alberto The FEBS Journal, Vol. 274, Issue 4 https://doi.org/10.1111/j.1742-4658.2007.05662.x	journal	January 2007
Siderophore-Based Iron Acquisition and Pathogen Control Miethke, M.; Marahiel, M. A. Microbiology and Molecular Biology Reviews, Vol. 71, Issue 3 https://doi.org/10.1128/MMBR.00012-07	journal	September 2007
Rapid and widespread dispersal of flood sediment on the northern California margin Wheatcroft, R. A.; Sommerfield, C. K.; Drake, D. E. Geology, Vol. 25, Issue 2 https://doi.org/10.1130/0091-7613(1997)025<0163:RAWDOF>2.3.CO;2	journal	January 1997
Chemistry of Marine Ligands and Siderophores Vraspir, Julia M.; Butler, Alison Annual Review of Marine Science, Vol. 1, Issue 1 https://doi.org/10.1146/annurev.marine.010908.163712	journal	January 2009
Evidence for phytoplankton iron limitation in the southern California Current System King, Al; Barbeau, K. Marine Ecology Progress Series, Vol. 342 https://doi.org/10.3354/meps342091	journal	July 2007
Distinct Siderophores Contribute to Iron Cycling in the Mesopelagic at Station ALOHA Bundy, Randelle M.; Boiteau, Rene M.; McLean, Craig Frontiers in Marine Science, Vol. 5 https://doi.org/10.3389/fmars.2018.00061	journal	March 2018
The organic complexation of iron in the marine environment: a review Gledhill, Martha Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00069	journal	January 2012
Iron and macronutrients in California coastal upwelling regimes: Implications for diatom blooms Bruland, Kenneth W.; Rue, Eden L.; Smith, Geoffrey J. Limnology and Oceanography, Vol. 46, Issue 7 https://doi.org/10.4319/lo.2001.46.7.1661	journal	November 2001
Structure of synechobactins, new siderophores of the marine cyanobacterium Synechococcus sp. PCC 7002 Ito, Yusai; Butler, Alison Limnology and Oceanography, Vol. 50, Issue 6 https://doi.org/10.4319/lo.2005.50.6.1918	journal	November 2005
The role of unchelated Fe in the iron nutrition of phytoplankton Morel, F. M. M.; Kustka, A. B.; Shaked, Y. Limnology and Oceanography, Vol. 53, Issue 1 https://doi.org/10.4319/lo.2008.53.1.0400	journal	January 2008
Saltmarshes as a source of chromophoric dissolved organic matter (CDOM) to Southern California coastal waters Clark, Catherine D.; Litz, Liannea P.; Grant, Stanley B. Limnology and Oceanography, Vol. 53, Issue 5 https://doi.org/10.4319/lo.2008.53.5.1923	journal	September 2008
Evidence for geochemical control of iron by humic substances in seawater Laglera, Luis M.; van den Berg, Constant M. G. Limnology and Oceanography, Vol. 54, Issue 2 https://doi.org/10.4319/lo.2009.54.2.0610	journal	March 2009
Distinct pools of dissolved iron-binding ligands in the surface and benthic boundary layer of the California Current Bundy, Randelle M.; Biller, Dondra V.; Buck, Kristen N. Limnology and Oceanography, Vol. 59, Issue 3 https://doi.org/10.4319/lo.2014.59.3.0769	journal	April 2014
Direct determination of iron in acidified (pH 1.7) seawater samples by flow injection analysis with catalytic spectrophotometric detection: Application and intercomparison: Direct determination of iron in seawater at pH 1.7 Lohan, Maeve C.; Aguilar-Islas, Ana M.; Bruland, Kenneth W. Limnology and Oceanography: Methods, Vol. 4, Issue 6 https://doi.org/10.4319/lom.2006.4.164	journal	June 2006
Molecular characterization of dissolved organic matter from subtropical wetlands: a comparative study through the analysis of optical properties, NMR and FTICR/MS Hertkorn, Norbert; Harir, Mourad; Cawley, Kaelin M. Biogeosciences, Vol. 13, Issue 8 https://doi.org/10.5194/bg-13-2257-2016	journal	January 2016
A comparison of biogenic iron quotas during a diatom spring bloom using multiple approaches King, A. L.; Sañudo-Wilhelmy, S. A.; Boyd, P. W. Biogeosciences, Vol. 9, Issue 2 https://doi.org/10.5194/bg-9-667-2012	journal	January 2012
Molecular characterization of dissolved organic matter from subtropical wetlands: a comparative study through the analysis of optical properties, NMR and FTICR/MS Hertkorn, N.; Harir, M.; Cawley, K. M. Biogeosciences Discussions, Vol. 12, Issue 16 https://doi.org/10.5194/bgd-12-13711-2015	journal	January 2015

Cited By (2)

Metallophores associated with Trichodesmium erythraeum colonies from the Gulf of Aqaba Gledhill, Martha; Basu, Subhajit; Shaked, Yeala Metallomics, Vol. 11, Issue 9 https://doi.org/10.1039/c9mt00121b	journal	January 2019
Reduction-dependent siderophore assimilation in a model pennate diatom Coale, Tyler H.; Moosburner, Mark; Horák, Aleš Proceedings of the National Academy of Sciences, Vol. 116, Issue 47 https://doi.org/10.1073/pnas.1907234116	journal	November 2019

Similar Records

Distinct Siderophores Contribute to Iron Cycling in the Mesopelagic at Station ALOHA

Journal Article · 2018 · Frontiers in Marine Science · OSTI ID:1426361

Bundy, Randelle M.; Boiteau, Rene M.; McLean, Craig; +5 more

Catalytic reduction of nitric oxide by the siderophore ferrioxamine B

Conference · 1995 · OSTI ID:126650

Smith, S R; Thorp, H H

The role of siderophores in the transport of radionuclides

Conference · 1993 · OSTI ID:62265

Hersman, L E; Palmer, P D; Hobart, D E

Related Subjects

54 ENVIRONMENTAL SCIENCES

Title: Patterns of iron and siderophore distributions across the California Current System

Citation Formats

References (61)

Cited By (2)

Similar Records

Related Subjects