Taxonomic and nutrient controls on phytoplankton iron quotas in the ocean

Twining, Benjamin S.; Antipova, Olga; Chappell, P. Dreux; Cohen, Natalie R.; Jacquot, Jeremy E.; Mann, Elizabeth L.; Marchetti, Adrian; Ohnemus, Daniel C.; Rauschenberg, Sara; Tagliabue, Alessandro

doi:10.1002/lol2.10179

Taxonomic and nutrient controls on phytoplankton iron quotas in the ocean

Journal Article · Tue Dec 29 00:00:00 EST 2020 · Limnology and Oceanography Letters

DOI:https://doi.org/10.1002/lol2.10179· OSTI ID:1752982

^[1]; Antipova, Olga ^[2]; ^[3]; Cohen, Natalie R. ^[4]; Jacquot, Jeremy E. ^[1]; Mann, Elizabeth L. ^[1]; ^[4]; Ohnemus, Daniel C. ^[1]; Rauschenberg, Sara ^[1]; ^[5]

Bigelow Laboratory for Ocean Sciences East Boothbay Maine USA
X‐ray Science Division, Advanced Photon Source Argonne National Laboratory Lemont Illinois USA
Department of Ocean, Earth and Atmospheric Sciences Old Dominion University Norfolk Virginia USA
Department of Marine Sciences University of North Carolina at Chapel Hill Chapel Hill North Carolina USA
School of Environmental Sciences University of Liverpool Liverpool UK

Abstract

Phytoplankton iron contents (i.e., quotas) directly link biogeochemical cycles of iron and carbon and drive patterns of nutrient limitation, recycling, and export. Ocean biogeochemical models typically assume that iron quotas are either static or controlled by dissolved iron availability. We measured iron quotas in phytoplankton communities across nutrient gradients in the Pacific Ocean and found that quotas diverged significantly in taxon‐specific ways from laboratory‐derived predictions. Iron quotas varied 40‐fold across nutrient gradients, and nitrogen‐limitation allowed diatoms to accumulate fivefold more iron than co‐occurring flagellates even under low iron availability. Modeling indicates such “luxury” uptake is common in large regions of the low‐iron Pacific Ocean. Among diatoms, both pennate and centric genera accumulated luxury iron, but the cosmopolitan pennate genus Pseudo‐nitzschia maintained iron quotas 10‐fold higher than co‐occurring centric diatoms, likely due to enhanced iron storage. Biogeochemical models should account for taxonomic and macronutrient controls on phytoplankton iron quotas.

View Journal Article

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

Sponsoring Organization:: European Research Council (ERC); National Science Foundation (NSF); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1752982

Alternate ID(s):: OSTI ID: 1838928
OSTI ID: 1786586

Journal Information:: Limnology and Oceanography Letters, Journal Name: Limnology and Oceanography Letters Journal Issue: 2 Vol. 6; ISSN 2378-2242

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United States

Language:: English

References (35)

How well do global ocean biogeochemistry models simulate dissolved iron distributions?: GLOBAL IRON MODELS Tagliabue, Alessandro; Aumont, Olivier; DeAth, Ros Global Biogeochemical Cycles, Vol. 30, Issue 2 https://doi.org/10.1002/2015GB005289	journal	February 2016
Iron Marchetti, Adrian; Maldonado, Maria T. The Physiology of Microalgae https://doi.org/10.1007/978-3-319-24945-2_11	book	January 2016
Iron uptake and growth limitation in oceanic and coastal phytoplankton Sunda, William G.; Huntsman, Susan A. Marine Chemistry, Vol. 50, Issue 1-4 https://doi.org/10.1016/0304-4203(95)00035-P	journal	August 1995
Chemical fractionation of phosphorus and cadmium in the marine diatom Phaeodactylum tricornutum Kudo, Isao; Kokubun, Haruyo; Matsunaga, Katsuhiko Marine Chemistry, Vol. 52, Issue 3-4 https://doi.org/10.1016/0304-4203(95)00086-0	journal	May 1996
What controls dissolved iron concentrations in the world ocean? Johnson, Kenneth S.; Gordon, R. Michael; Coale, Kenneth H. Marine Chemistry, Vol. 57, Issue 3-4 https://doi.org/10.1016/S0304-4203(97)00043-1	journal	July 1997
Spatial patterns of nitrogen uptake and phytoplankton in the equatorial upwelling zone (110°W–140°W) during 2004 and 2005 Parker, Alexander E.; Wilkerson, Frances P.; Dugdale, Richard C. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 58, Issue 3-4 https://doi.org/10.1016/j.dsr2.2010.08.013	journal	February 2011
Global-scale carbon and energy flows through the marine planktonic food web: An analysis with a coupled physical–biological model Stock, Charles A.; Dunne, John P.; John, Jasmin G. Progress in Oceanography, Vol. 120 https://doi.org/10.1016/j.pocean.2013.07.001	journal	January 2014
Metal contents of phytoplankton and labile particulate material in the North Atlantic Ocean Twining, Benjamin S.; Rauschenberg, Sara; Morton, Peter L. Progress in Oceanography, Vol. 137 https://doi.org/10.1016/j.pocean.2015.07.001	journal	September 2015
Upper ocean ecosystem dynamics and iron cycling in a global three-dimensional model: GLOBAL ECOSYSTEM-BIOGEOCHEMICAL MODEL Moore, J. Keith; Doney, Scott C.; Lindsay, Keith Global Biogeochemical Cycles, Vol. 18, Issue 4 https://doi.org/10.1029/2004GB002220	journal	December 2004
Synthesis of iron fertilization experiments: From the Iron Age in the Age of Enlightenment de Baar, Hein J. W. Journal of Geophysical Research, Vol. 110, Issue C9 https://doi.org/10.1029/2004JC002601	journal	January 2005
The decoupling of production and particulate export in the surface ocean Buesseler, Ken O. Global Biogeochemical Cycles, Vol. 12, Issue 2 https://doi.org/10.1029/97GB03366	journal	June 1998
Low iron requirement for growth in oceanic phytoplankton Sunda, William G.; Swift, Dorothy G.; Huntsman, Susan A. Nature, Vol. 351, Issue 6321 https://doi.org/10.1038/351055a0	journal	May 1991
Interrelated influence of iron, light and cell size on marine phytoplankton growth Sunda, William G.; Huntsman, Susan A. Nature, Vol. 390, Issue 6658 https://doi.org/10.1038/37093	journal	November 1997
The evolutionary inheritance of elemental stoichiometry in marine phytoplankton Quigg, Antonietta; Finkel, Zoe V.; Irwin, Andrew J. Nature, Vol. 425, Issue 6955 https://doi.org/10.1038/nature01953	journal	September 2003
Ferritin is used for iron storage in bloom-forming marine pennate diatoms Marchetti, Adrian; Parker, Micaela S.; Moccia, Lauren P. Nature, Vol. 457, Issue 7228 https://doi.org/10.1038/nature07539	journal	November 2008
Nutrient co-limitation at the boundary of an oceanic gyre Browning, Thomas J.; Achterberg, Eric P.; Rapp, Insa Nature, Vol. 551, Issue 7679 https://doi.org/10.1038/nature24063	journal	November 2017
Processes and patterns of oceanic nutrient limitation Moore, C. M.; Mills, M. M.; Arrigo, K. R. Nature Geoscience, Vol. 6, Issue 9 https://doi.org/10.1038/ngeo1765	journal	March 2013
Recycled iron fuels new production in the eastern equatorial Pacific Ocean Rafter, Patrick A.; Sigman, Daniel M.; Mackey, Katherine R. M. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01219-7	journal	October 2017
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
Different iron storage strategies among bloom-forming diatoms Lampe, Robert H.; Mann, Elizabeth L.; Cohen, Natalie R. Proceedings of the National Academy of Sciences, Vol. 115, Issue 52 https://doi.org/10.1073/pnas.1805243115	journal	December 2018
An iron cycle cascade governs the response of equatorial Pacific ecosystems to climate change Tagliabue, Alessandro; Barrier, Nicolas; Du Pontavice, Hubert Global Change Biology, Vol. 26, Issue 11 https://doi.org/10.1111/gcb.15316	journal	September 2020
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
Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions Boyd, P. W.; Jickells, T.; Law, C. S. Science, Vol. 315, Issue 5812 https://doi.org/10.1126/science.1131669	journal	February 2007
Diversity and Evolutionary History of Iron Metabolism Genes in Diatoms Groussman, Ryan D.; Parker, Micaela S.; Armbrust, E. Virginia PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0129081	journal	June 2015
Patterns of diatom diversity correlate with dissolved trace metal concentrations and longitudinal position in the northeast Pacific coastal-offshore transition zone Chappell, Pd; Armbrust, Ev; Barbeau, Ka Marine Ecology Progress Series, Vol. 609 https://doi.org/10.3354/meps12810	journal	January 2019
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
Diatom Transcriptional and Physiological Responses to Changes in Iron Bioavailability across Ocean Provinces Cohen, Natalie R.; Ellis, Kelsey A.; Lampe, Robert H. Frontiers in Marine Science, Vol. 4 https://doi.org/10.3389/fmars.2017.00360	journal	November 2017
Prey Stoichiometry Drives Iron Recycling by Zooplankton in the Global Ocean Richon, Camille; Aumont, Olivier; Tagliabue, Alessandro Frontiers in Marine Science, Vol. 7 https://doi.org/10.3389/fmars.2020.00451	journal	June 2020
The equatorial Pacific Ocean: Grazer-controlled phytoplankton populations in an iron-limited ecosystem1 Price, N. M.; Ahner, B. A.; Morel, F. M. M. Limnology and Oceanography, Vol. 39, Issue 3 https://doi.org/10.4319/lo.1994.39.3.0520	journal	May 1994
The incorporation of zinc and iron into the frustule of the marine diatom Thalassiosira pseudonana Ellwood, Michael J.; Hunter, Keith A. Limnology and Oceanography, Vol. 45, Issue 7 https://doi.org/10.4319/lo.2000.45.7.1517	journal	November 2000
Effect of iron limitation on the cadmium to phosphorus ratio of natural phytoplankton assemblages from the Southern Ocean Cullen, Jay T.; Chase, Zanna; Coale, Kenneth H. Limnology and Oceanography, Vol. 48, Issue 3 https://doi.org/10.4319/lo.2003.48.3.1079	journal	May 2003
Iron requirements of the pennate diatom Pseudo-nitzschia : Comparison of oceanic (high-nitrate, low-chlorophyll waters) and coastal species Marchetti, Adrian; Maldonado, Maria T.; Lane, Erin S. Limnology and Oceanography, Vol. 51, Issue 5 https://doi.org/10.4319/lo.2006.51.5.2092	journal	September 2006
A model of phytoplankton acclimation to iron-light colimitation Buitenhuis, Erik T.; Geider, Richard J. Limnology and Oceanography, Vol. 55, Issue 2 https://doi.org/10.4319/lo.2010.55.2.0714	journal	February 2010
Adaptive strategies by Southern Ocean phytoplankton to lessen iron limitation: Uptake of organically complexed iron and reduced cellular iron requirements Strzepek, Robert F.; Maldonado, Maria T.; Hunter, Keith A. Limnology and Oceanography, Vol. 56, Issue 6 https://doi.org/10.4319/lo.2011.56.6.1983	journal	September 2011
PISCES-v2: an ocean biogeochemical model for carbon and ecosystem studies Aumont, O.; Ethé, C.; Tagliabue, A. Geoscientific Model Development, Vol. 8, Issue 8 https://doi.org/10.5194/gmd-8-2465-2015	journal	January 2015

Similar Records

Trace metal contents of autotrophic flagellates from contrasting open‐ocean ecosystems

Journal Article · Wed May 25 20:00:00 EDT 2022 · Limnology and Oceanography Letters · OSTI ID:1870025

Related Subjects

54 ENVIRONMENTAL SCIENCES

Taxonomic and nutrient controls on phytoplankton iron quotas in the ocean

Citation Formats

References (35)

Similar Records

Related Subjects