Pervasive iron limitation at subsurface chlorophyll maxima of the California Current

Significance The vertical distribution of phytoplankton cells and chlorophyll concentrations throughout the sunlit water column is rarely uniform. In many ocean regions, chlorophyll concentrations peak in distinct and persistent layers deep below the surface called subsurface chlorophyll maximum layers (SCMLs). SCML formation is hypothesized to reflect the consequences of phytoplankton light/macronutrient colimitation, behavior, and/or photoacclimation. We discovered unexpectedly persistent and widespread phytoplankton iron limitation and iron/light colimitation in SCMLs of the California Current and at the edge of the North Pacific Subtropical Gyre using shipboard incubations, metatranscriptomics, and biogeochemical proxies. These results suggest that interactions and feedbacks between iron and light availability play an important and previously unrecognized role in controlling the productivity and biogeochemical dynamics of SCMLs. Subsurface chlorophyll maximum layers (SCMLs) are nearly ubiquitous in stratified water columns and exist at horizontal scales ranging from the submesoscale to the extent of oligotrophic gyres. These layers of heightened chlorophyll and/or phytoplankton concentrations are generally thought to be a consequence of a balance between light energy from above and a limiting nutrient flux from below, typically nitrate (NO3). Here we present multiple lines of evidence demonstrating that iron (Fe) limits or with light colimits phytoplankton communities in SCMLs along a primary productivity gradient from coastal to oligotrophic offshore waters in the southern California Current ecosystem. SCML phytoplankton responded markedly to added Fe or Fe/light in experimental incubations and transcripts of diatom and picoeukaryote Fe stress genes were strikingly abundant in SCML metatranscriptomes. Using a biogeochemical proxy with data from a 40-y time series, we find that diatoms growing in California Current SCMLs are persistently Fe deficient during the spring and summer growing season. We also find that the spatial extent of Fe deficiency within California Current SCMLs has significantly increased over the last 25 y in line with a regional climate index. Finally, we show that diatom Fe deficiency may be common in the subsurface of major upwelling zones worldwide. Our results have important implications for our understanding of the biogeochemical consequences of marine SCML formation and maintenance.

[1]  M. Brzezinski,et al.  THE Si:C:N RATIO OF MARINE DIATOMS: INTERSPECIFIC VARIABILITY AND THE EFFECT OF SOME ENVIRONMENTAL VARIABLES 1 , 1985 .

[2]  James J. Simpson,et al.  The California Current system: The seasonal variability of its physical characteristics , 1987 .

[3]  J. Raven.  Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway , 1990 .

[4]  D. Hutchins,et al.  Interactive influences of bioactive trace metals on biological production in oceanic waters , 1991 .

[5]  Lynne D. Talley,et al.  An Okhotsk Sea water anomaly: implications for ventilation in the North Pacific , 1991 .

[6]  D. Tilman,et al.  Plant Allocation and the Multiple Limitation Hypothesis , 1992, The American Naturalist.

[7]  A. J. Watson,et al.  Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean , 1994, Nature.

[8]  K. Bruland,et al.  Complexation of iron(III) by natural organic ligands in the Central North Pacific as determined by a new competitive ligand equilibration/adsorptive cathodic stripping voltammetric method , 1995 .

[9]  W. Sunda,et al.  Iron uptake and growth limitation in oceanic and coastal phytoplankton , 1995 .

[10]  K. Bruland,et al.  The role of organic complexation on ambient iron chemistry in the equatorial Pacific Ocean and the response of a mesoscale iron addition experiment , 1997 .

[11]  Nicolas Gruber,et al.  Global patterns of marine nitrogen fixation and denitrification , 1997 .

[12]  W. Sunda,et al.  Interrelated influence of iron, light and cell size on marine phytoplankton growth , 1997, Nature.

[13]  D. Hutchins,et al.  Iron-limited diatom growth and Si:N uptake ratios in a coastal upwelling regime , 1998, Nature.

[14]  Shigenobu Takeda,et al.  Influence of iron availability on nutrient consumption ratio of diatoms in oceanic waters , 1998, Nature.

[15]  P. Boyd,et al.  Co-limitation of phytoplankton growth by light and Fe during winter in the NE subarctic Pacific Ocean , 1999 .

[16]  M. Kahru,et al.  Influence of the 1997–98 El Niño on the surface chlorophyll in the California Current , 2000 .

[17]  D. M. Nelson,et al.  Iron and silicic acid concentrations regulate Si uptake north and south of the Polar Frontal Zone in the Pacific Sector of the Southern Ocean , 2000 .

[18]  S. Doney,et al.  Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean , 2001 .

[19]  B. Quéguiner,et al.  Control of phytoplankton growth by iron and silicic acid availability in the subantarctic Southern Ocean: Experimental results from the SAZ Project , 2001 .

[20]  B. Quéguiner,et al.  Control of phytoplankton growth by iron supply and irradiance in the subantarctic Southern Ocean: Experimental results from the SAZ Project , 2001 .

[21]  Kenneth W. Bruland,et al.  Iron and macronutrients in California coastal upwelling regimes: Implications for diatom blooms , 2001 .

[22]  M. Brzezinski,et al.  Silicic acid leakage from the Southern Ocean: A possible explanation for glacial atmospheric pCO2 , 2002 .

[23]  Giacomo R. DiTullio,et al.  Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling , 2002 .

[24]  S. Tsunogai.  The Western North Pacific Playing a Key Role in Global Biogeochemical Fluxes , 2002 .

[25]  Emanuele Di Lorenzo,et al.  Seasonal dynamics of the surface circulation in the Southern California Current System , 2003 .

[26]  S. Bograd,et al.  Long-term variability in the Southern California Current System , 2003 .

[27]  Edward J. Kearns,et al.  Production regimes in four Eastern Boundary Current systems , 2003 .

[28]  K. Arrigo.  Marine microorganisms and global nutrient cycles , 2005, Nature.

[29]  M. Brzezinski,et al.  High-latitude controls of thermocline nutrients and low latitude biological productivity , 2004, Nature.

[30]  P. Harrison,et al.  Photosynthetic architecture differs in coastal and oceanic diatoms , 2004, Nature.

[31]  William Miller,et al.  The decline and fate of an iron-induced subarctic phytoplankton bloom , 2004, Nature.

[32]  S. Bograd,et al.  On the subduction of upwelled waters in the California Current , 2005 .

[33]  Simon J. Ussher,et al.  Iron in the Sargasso Sea (Bermuda Atlantic Time‐series Study region) during summer: Eolian imprint, spatiotemporal variability, and ecological implications , 2005 .

[34]  E. Boyle,et al.  Iron, manganese, and lead at Hawaii Ocean Time-series station ALOHA: Temporal variability and an intermediate water hydrothermal plume , 2005 .

[35]  K. Bruland,et al.  The physicochemical speciation of dissolved iron in the Bering Sea, Alaska , 2007 .

[36]  A. King,et al.  Evidence for phytoplankton iron limitation in the southern California Current System , 2007 .

[37]  E. Boyle,et al.  Mesoscale Iron Enrichment Experiments 1993-2005: Synthesis and Future Directions , 2007, Science.

[38]  K. Bruland,et al.  Dissolved iron speciation in two distinct river plumes and an estuary: Implications for riverine iron supply , 2007 .

[39]  S. J. Tanner,et al.  Developing standards for dissolved iron in seawater , 2007 .

[40]  James C. McWilliams,et al.  North Pacific Gyre Oscillation links ocean climate and ecosystem change , 2008 .

[41]  R. Rykaczewski,et al.  Influence of ocean winds on the pelagic ecosystem in upwelling regions , 2008, Proceedings of the National Academy of Sciences.

[42]  Alejandro A. Schäffer,et al.  Database indexing for production MegaBLAST searches , 2008, Bioinform..

[43]  A. Fernie,et al.  Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation , 2008, Proceedings of the National Academy of Sciences.

[44]  K. Barbeau,et al.  Interactive influences of iron and light limitation on phytoplankton at subsurface chlorophyll maxima in the eastern North Pacific , 2008 .

[45]  Jason T. Ritt,et al.  Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability , 2008 .

[46]  E. Virginia Armbrust,et al.  Ferritin is used for iron storage in bloom-forming marine pennate diatoms , 2009, Nature.

[47]  F. Chavez,et al.  Potential new production estimates in four eastern boundary upwelling ecosystems , 2009 .

[48]  Mark D. Ohman,et al.  Multi‐decadal shoaling of the euphotic zone in the southern sector of the California Current System , 2009 .

[49]  John P. Dunne,et al.  Enhanced nutrient supply to the California Current Ecosystem with global warming and increased stratification in an earth system model , 2010 .

[50]  Haixu Tang,et al.  FragGeneScan: predicting genes in short and error-prone reads , 2010, Nucleic acids research.

[51]  Z. Johnson,et al.  The effect of iron- and light-limitation on phytoplankton communities of deep chlorophyll maxima of the western Pacific Ocean , 2010 .

[52]  Limin Fu,et al.  Artificial and natural duplicates in pyrosequencing reads of metagenomic data , 2010, BMC Bioinformatics.

[53]  A. Santoro,et al.  Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. , 2010, Environmental microbiology.

[54]  E. Delong,et al.  Development and quantitative analyses of a universal rRNA-subtraction protocol for microbial metatranscriptomics , 2010, The ISME Journal.

[55]  James C. McWilliams,et al.  Eddy-induced reduction of biological production in eastern boundary upwelling systems , 2011 .

[56]  A. King,et al.  Dissolved iron and macronutrient distributions in the southern California Current System , 2011 .

[57]  Peter Williams,et al.  IMG: the integrated microbial genomes database and comparative analysis system , 2011, Nucleic Acids Res..

[58]  David M Schruth,et al.  Comparative metatranscriptomics identifies molecular bases for the physiological responses of phytoplankton to varying iron availability , 2012, Proceedings of the National Academy of Sciences.

[59]  Osvaldo Ulloa,et al.  Microbial oceanography of anoxic oxygen minimum zones , 2012, Proceedings of the National Academy of Sciences.

[60]  P. Boyd,et al.  Iron‐light interactions differ in Southern Ocean phytoplankton , 2012 .

[61]  A. King,et al.  Quasi-Lagrangian drifter studies of iron speciation and cycling off Point Conception, California , 2012 .

[62]  M. Kahru,et al.  Pelagic community responses to a deep-water front in the California Current Ecosystem: overview of the A-Front Study , 2012 .

[63]  M. Ohman,et al.  A double-integration hypothesis to explain ocean ecosystem response to climate forcing , 2013, Proceedings of the National Academy of Sciences.

[64]  K. Arrigo,et al.  Processes and patterns of oceanic nutrient limitation , 2013 .

[65]  Timothy P. Boyer,et al.  World ocean atlas 2013. Volume 4, Dissolved inorganic nutrients (phosphate, nitrate, silicate) , 2013 .

[66]  R. Goericke,et al.  Ecological transitions in a coastal upwelling ecosystem , 2013 .

[67]  K. Johnson,et al.  Measurements of nitrite production in and around the primary nitrite maximum in the central California Current , 2013 .

[68]  David S. Matteson,et al.  ecp: An R Package for Nonparametric Multiple Change Point Analysis of Multivariate Data , 2013, 1309.3295.

[69]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[70]  Susumu Goto,et al.  Data, information, knowledge and principle: back to metabolism in KEGG , 2013, Nucleic Acids Res..

[71]  P. Sedwick,et al.  The organic complexation of dissolved iron along the U.S. GEOTRACES (GA03) North Atlantic Section , 2015 .

[72]  T. Goepfert,et al.  Biogeochemistry of iron in the Arabian Sea , 2015 .

[73]  R. Rykaczewski,et al.  Anticipated Effects of Climate Change on Coastal Upwelling Ecosystems , 2015, Current Climate Change Reports.

[74]  Alaguraj Veluchamy,et al.  A Novel Protein, Ubiquitous in Marine Phytoplankton, Concentrates Iron at the Cell Surface and Facilitates Uptake , 2015, Current Biology.

[75]  A. Oschlies,et al.  Enhanced sensitivity of oceanic CO2 uptake to dust deposition by iron‐light colimitation , 2015 .

[76]  Mercedes Pozo Buil,et al.  Changes in source waters to the Southern California Bight , 2015 .

[77]  Elizabeth L. Mann,et al.  Genomes and gene expression across light and productivity gradients in eastern subtropical Pacific microbial communities , 2014, The ISME Journal.

[78]  P. Franks,et al.  A pseudo‐Lagrangian method for remapping ocean biogeochemical tracer data: Calculation of net Chl‐a growth rates , 2015 .

[79]  A. Marchetti,et al.  Marine diatom proteorhodopsins and their potential role in coping with low iron availability , 2015, The ISME Journal.

[80]  Tom O. Delmont,et al.  Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge , 2015, Proceedings of the National Academy of Sciences.

[81]  LeAnn P. Whitney,et al.  Genetic indicators of iron limitation in wild populations of Thalassiosira oceanica from the northeast Pacific Ocean , 2014, The ISME Journal.

[82]  M. Brzezinski,et al.  Enhanced silica ballasting from iron stress sustains carbon export in a frontal zone within the California Current , 2015 .

[83]  S. Hogle,et al.  Copiotrophic marine bacteria are associated with strong iron‐binding ligand production during phytoplankton blooms , 2016 .

[84]  Dan M. Bolser,et al.  Ensembl Genomes 2016: more genomes, more complexity , 2015, Nucleic Acids Res..

[85]  D. Checkley,et al.  Resilience and stability of a pelagic marine ecosystem , 2016, Proceedings of the Royal Society B: Biological Sciences.

[86]  D. Raubenheimer,et al.  Bridging factorial and gradient concepts of resource co-limitation: towards a general framework applied to consumers. , 2016, Ecology letters.

[87]  Alexander M. Chekalyuk,et al.  Mesoscale ocean fronts enhance carbon export due to gravitational sinking and subduction , 2017, Proceedings of the National Academy of Sciences.

[88]  George Sugihara,et al.  Predicting coastal algal blooms in southern California. , 2017, Ecology.

[89]  K. Johnson,et al.  The integral role of iron in ocean biogeochemistry , 2017, Nature.

[90]  M. Brzezinski,et al.  Diatom Transcriptional and Physiological Responses to Changes in Iron Bioavailability across Ocean Provinces , 2017, Front. Mar. Sci..

[91]  Decadal dynamics and predictability of oxygen and subsurface tracers in the California Current System , 2017 .

[92]  E. Achterberg,et al.  Nutrient co-limitation at the boundary of an oceanic gyre , 2017, Nature.

[93]  J. Venter,et al.  The Baltic Sea Virome: Diversity and Transcriptional Activity of DNA and RNA Viruses , 2017, mSystems.

[94]  P. Boyd,et al.  Biotic and abiotic retention, recycling and remineralization of metals in the ocean , 2017 .

[95]  N. Cohen,et al.  Development of a molecular‐based index for assessing iron status in bloom‐forming pennate diatoms , 2017, Journal of phycology.

[96]  M. Lomas,et al.  Ambient nitrate switches the ammonium consumption pathway in the euphotic ocean , 2018, Nature Communications.

[97]  Bogumil J. Karas,et al.  Carbonate-sensitive phytotransferrin controls high-affinity iron uptake in diatoms , 2018, Nature.

[98]  M. Sakata,et al.  High-latitude controls of thermocline nutrients and low latitude biological productivity , 2022 .