Modest net autotrophy in the oligotrophic ocean

Letscher, Robert T.; Moore, J. Keith

doi:10.1002/2016GB005503

Modest net autotrophy in the oligotrophic ocean

Journal Article · Sat Apr 01 00:00:00 EDT 2017 · Global Biogeochemical Cycles

DOI:https://doi.org/10.1002/2016GB005503· OSTI ID:1465338

^[1]; Moore, J. Keith ^[2]

Univ. of California, Irvine, CA (United States). Earth System Science; University of California, Irvine
Univ. of California, Irvine, CA (United States). Earth System Science

The metabolic state of the oligotrophic subtropical ocean has long been debated. Net community production (NCP) represents the balance of autotrophic carbon fixation with heterotrophic respiration. Many in vitro NCP estimates based on oxygen incubation methods and the corresponding scaling relationships used to predict the ecosystem metabolic balance have suggested the ocean gyres to be net heterotrophic; however, all in situ NCP methods find net autotrophy. Reconciling net heterotrophy requires significant allochthonous inputs of organic carbon to the oligotrophic gyres to sustain a preponderance of respiration over in situ production. Here we use the first global ecosystem-ocean circulation model that contains representation of the three allochthonous carbon sources to the open ocean, to show that the five oligotrophic gyres exhibit modest net autotrophy throughout the seasonal cycle. Annually integrated rates of NCP vary in the range ~1.5–2.2 mol O₂ m^-2 yr^-1 across the five gyre systems; however, seasonal NCP rates are as low as ~1 ± 0.5 mmol O2 m^-2 d^-1 for the North Atlantic. Volumetric NCP rates are heterotrophic below the 10% light level; however, they become net autotrophic when integrated over the euphotic zone. Observational uncertainties when measuring these modest autotrophic NCP rates as well as the metabolic diversity encountered across space and time complicate the scaling up of in vitro measurements to the ecosystem scale and may partially explain the previous reports of net heterotrophy. The oligotrophic ocean is autotrophic at present; however, it could shift toward seasonal heterotrophy in the future as rising temperatures stimulate respiration.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of California, Irvine, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0012550

OSTI ID:: 1465338

Alternate ID(s):: OSTI ID: 1402335

Journal Information:: Global Biogeochemical Cycles, Journal Name: Global Biogeochemical Cycles Journal Issue: 4 Vol. 31; ISSN 0886-6236

Publisher:: American Geophysical Union (AGU)Copyright Statement

Country of Publication:: United States

Language:: English

References (54)

Annual net community production and the biological carbon flux in the ocean: OCEAN BIOLOGICAL ORGANIC CARBON FLUX Emerson, Steven Global Biogeochemical Cycles, Vol. 28, Issue 1 https://doi.org/10.1002/2013GB004680	journal	January 2014
Preferential remineralization of dissolved organic phosphorus and non-Redfield DOM dynamics in the global ocean: Impacts on marine productivity, nitrogen fixation, and carbon export Letscher, Robert T.; Moore, J. Keith Global Biogeochemical Cycles, Vol. 29, Issue 3 https://doi.org/10.1002/2014GB004904	journal	March 2015
A reevaluation of the magnitude and impacts of anthropogenic atmospheric nitrogen inputs on the ocean: Atmospheric nitrogen inputs Jickells, T. D.; Buitenhuis, E.; Altieri, K. Global Biogeochemical Cycles https://doi.org/10.1002/2016GB005586	journal	January 2017
Effects of increased isopycnal diffusivity mimicking the unresolved equatorial intermediate current system in an earth system climate model: MIMICKING THE EICS Getzlaff, Julia; Dietze, Heiner Geophysical Research Letters, Vol. 40, Issue 10 https://doi.org/10.1002/grl.50419	journal	May 2013
Bacteria and Marine Biogeochemistry Jørgensen, Bo Barker Marine Geochemistry https://doi.org/10.1007/3-540-32144-6_5	book	January 2006
Large-Scale, Persistent Nutrient Fronts of the World Ocean: Impacts on Biogeochemistry Palter, Jaime B.; Marinov, Irina; Sarmiento, Jorge L. Chemical Oceanography of Frontal Zones https://doi.org/10.1007/698_2013_241	book	January 2013
Seasonal patterns of ocean biogeochemistry at the U.S. JGOFS Bermuda Atlantic time-series study site Michaels, Anthony F.; Knap, Anthony H.; Dow, Rachael L. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 41, Issue 7 https://doi.org/10.1016/0967-0637(94)90016-7	journal	July 1994
Seasonal and interannual variability of oceanic carbon dioxide species at the U.S. JGOFS Bermuda Atlantic Time-series Study (BATS) site Bates, Nicholas R.; Michaels, Anthony F.; Knap, Anthony H. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 43, Issue 2-3 https://doi.org/10.1016/0967-0645(95)00093-3	journal	January 1996
Seasonal patterns of ocean biogeochemistry at the U.S. JGOFS Bermuda Atlantic time-series study site Michaels, Anthony F.; Knap, Anthony H.; Dow, Rachael L. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 41, Issue 7 https://doi.org/10.1016/0967‐0637(94)90016‐7	journal	July 1994
Seasonal and interannual variability of oceanic carbon dioxide species at the U.S. JGOFS Bermuda Atlantic Time-series Study (BATS) site Bates, Nicholas R.; Michaels, Anthony F.; Knap, Anthony H. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 43, Issue 2-3 https://doi.org/10.1016/0967‐0645(95)00093‐3	journal	January 1996
Surface layer carbon budget for the subtropical N. Pacific: constraints at station ALOHA Quay, Paul; Stutsman, John Deep Sea Research Part I: Oceanographic Research Papers, Vol. 50, Issue 9 https://doi.org/10.1016/S0967-0637(03)00116-X	journal	September 2003
Carbon-13 constraints on the seasonal inorganic carbon budget at the BATS site in the northwestern Sargasso Sea Gruber, Nicolas; Keeling, Charles D.; Stocker, Thomas F. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 45, Issue 4-5 https://doi.org/10.1016/S0967-0637(97)00098-8	journal	April 1998
Carbon-13 constraints on the seasonal inorganic carbon budget at the BATS site in the northwestern Sargasso Sea Gruber, Nicolas; Keeling, Charles D.; Stocker, Thomas F. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 45, Issue 4-5 https://doi.org/10.1016/S0967‐0637(97)00098‐8	journal	April 1998
Production and respiration control the marine microbial metabolic balance in the eastern North Atlantic subtropical gyre Aranguren-Gassis, María; Serret, Pablo; Fernández, Emilio Deep Sea Research Part I: Oceanographic Research Papers, Vol. 58, Issue 7 https://doi.org/10.1016/j.dsr.2011.05.003	journal	July 2011
Subtropical gyre variability observed by ocean-color satellites McClain, Charles R.; Signorini, Sergio R.; Christian, James R. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 51, Issue 1-3 https://doi.org/10.1016/j.dsr2.2003.08.002	journal	January 2004
Seasonal and spatial variability in plankton production and respiration in the Subtropical Gyres of the Atlantic Ocean Gist, Niki; Serret, Pablo; Woodward, E. M. S. Deep Sea Research Part II: Topical Studies in Oceanography, Vol. 56, Issue 15 https://doi.org/10.1016/j.dsr2.2008.10.035	journal	July 2009
Global Nutrient Export from WaterSheds 2 (NEWS 2): Model development and implementation Mayorga, Emilio; Seitzinger, Sybil P.; Harrison, John A. Environmental Modelling & Software, Vol. 25, Issue 7 https://doi.org/10.1016/j.envsoft.2010.01.007	journal	July 2010
An offline implicit solver for simulating prebomb radiocarbon Bardin, Ann; Primeau, François; Lindsay, Keith Ocean Modelling, Vol. 73 https://doi.org/10.1016/j.ocemod.2013.09.008	journal	January 2014
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
Seasonal and long-term dynamics of the upper ocean carbon cycle at Station ALOHA near Hawaii: SEASONAL CYCLES AND TRENDS AT STATION ALOHA Keeling, Charles D.; Brix, Holger; Gruber, Nicolas Global Biogeochemical Cycles, Vol. 18, Issue 4 https://doi.org/10.1029/2004GB002227	journal	October 2004
Ocean's least productive waters are expanding Polovina, Jeffrey J.; Howell, Evan A.; Abecassis, Melanie Geophysical Research Letters, Vol. 35, Issue 3 https://doi.org/10.1029/2007GL031745	journal	January 2008
Distribution of dissolved organic nutrients and their effect on export production over the Atlantic Ocean: DON AND DOP IN THE ATLANTIC OCEAN Torres-Valdés, S.; Roussenov, V. M.; Sanders, R. Global Biogeochemical Cycles, Vol. 23, Issue 4 https://doi.org/10.1029/2008GB003389	journal	November 2009
Global river nutrient export: A scenario analysis of past and future trends: GLOBAL RIVER EXPORT SCENARIOS Seitzinger, S. P.; Mayorga, E.; Bouwman, A. F. Global Biogeochemical Cycles, Vol. 24, Issue 4 https://doi.org/10.1029/2009GB003587	journal	May 2010
Measuring primary production rates in the ocean: Enigmatic results between incubation and non-incubation methods at Station ALOHA: PRIMARY PRODUCTION RATES IN THE OCEAN Quay, P. D.; Peacock, C.; Björkman, K. Global Biogeochemical Cycles, Vol. 24, Issue 3 https://doi.org/10.1029/2009GB003665	journal	July 2010
Temperature dependence of planktonic metabolism in the ocean: PLANKTONIC METABOLISM Regaudie-de-Gioux, A.; Duarte, C. M. Global Biogeochemical Cycles, Vol. 26, Issue 1 https://doi.org/10.1029/2010GB003907	journal	February 2012
Global net community production and the putative net heterotrophy of the oligotrophic oceans: NET COMMUNITY PRODUCTION FROM SATELLITE Westberry, Toby K.; Williams, Peter J. le B.; Behrenfeld, Michael J. Global Biogeochemical Cycles, Vol. 26, Issue 4 https://doi.org/10.1029/2011GB004094	journal	December 2012
Atmospheric fluxes of organic N and P to the global ocean: ATMOSPHERIC ORGANIC N AND P TO THE OCEAN Kanakidou, Maria; Duce, Robert A.; Prospero, Joseph M. Global Biogeochemical Cycles, Vol. 26, Issue 3 https://doi.org/10.1029/2011GB004277	journal	September 2012
Chemoautotrophy in the ocean: CHEMOAUTOTROPHY IN THE OCEAN Middelburg, Jack J. Geophysical Research Letters, Vol. 38, Issue 24 https://doi.org/10.1029/2011GL049725	journal	December 2011
Redfield ratios of remineralization determined by nutrient data analysis Anderson, Laurence A.; Sarmiento, Jorge L. Global Biogeochemical Cycles, Vol. 8, Issue 1 https://doi.org/10.1029/93GB03318	journal	March 1994
Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems del Giorgio, Paul A.; Cole, Jonathan J.; Cimbleris, André Nature, Vol. 385, Issue 6612 https://doi.org/10.1038/385148a0	journal	January 1997
Experimental determination of the organic carbon flux from open-ocean surface waters Emerson, S.; Quay, P.; Karl, D. Nature, Vol. 389, Issue 6654 https://doi.org/10.1038/40111	journal	October 1997
Nutrient budgets in the subtropical ocean gyres dominated by lateral transport Letscher, Robert T.; Primeau, François; Moore, J. Keith Nature Geoscience, Vol. 9, Issue 11 https://doi.org/10.1038/ngeo2812	journal	October 2016
Scaling the metabolic balance of the oceans Lopez-Urrutia, A.; San Martin, E.; Harris, R. P. Proceedings of the National Academy of Sciences, Vol. 103, Issue 23 https://doi.org/10.1073/pnas.0601137103	journal	May 2006
Global fish production and climate change Brander, K. M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 50 https://doi.org/10.1073/pnas.0702059104	journal	December 2007
Genome analysis of the proteorhodopsin-containing marine bacterium Polaribacter sp. MED152 (Flavobacteria) Gonzalez, J. M.; Fernandez-Gomez, B.; Fernandez-Guerra, A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 25 https://doi.org/10.1073/pnas.0712027105	journal	June 2008
Stimulation of growth by proteorhodopsin phototrophy involves regulation of central metabolic pathways in marine planktonic bacteria Palovaara, J.; Akram, N.; Baltar, F. Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1402617111	journal	August 2014
Impacts of Atmospheric Anthropogenic Nitrogen on the Open Ocean Duce, R. A.; LaRoche, J.; Altieri, K. Science, Vol. 320, Issue 5878 https://doi.org/10.1126/science.1150369	journal	May 2008
The CO2 Balance of Unproductive Aquatic Ecosystems Duarte, C. M. Science, Vol. 281, Issue 5374 https://doi.org/10.1126/science.281.5374.234	journal	July 1998
The Oligotrophic Ocean Is Autotrophic Williams, Peter J. le B.; Quay, Paul D.; Westberry, Toby K. Annual Review of Marine Science, Vol. 5, Issue 1 https://doi.org/10.1146/annurev-marine-121211-172335	journal	January 2013
The Oligotrophic Ocean Is Heterotrophic Duarte, Carlos M.; Regaudie-de-Gioux, Aurore; Arrieta, Jesús M. Annual Review of Marine Science, Vol. 5, Issue 1 https://doi.org/10.1146/annurev-marine-121211-172337	journal	January 2013
The Oligotrophic Ocean Is Autotrophic Williams, Peter J. le B.; Quay, Paul D.; Westberry, Toby K. Annual Review of Marine Science, Vol. 5, Issue 1 https://doi.org/10.1146/annurev‐marine‐121211‐172335	journal	January 2013
The Oligotrophic Ocean Is Heterotrophic Duarte, Carlos M.; Regaudie-de-Gioux, Aurore; Arrieta, Jesús M. Annual Review of Marine Science, Vol. 5, Issue 1 https://doi.org/10.1146/annurev‐marine‐121211‐172337	journal	January 2013
Marine Ecosystem Dynamics and Biogeochemical Cycling in the Community Earth System Model [CESM1(BGC)]: Comparison of the 1990s with the 2090s under the RCP4.5 and RCP8.5 Scenarios Moore, J. Keith; Lindsay, Keith; Doney, Scott C. Journal of Climate, Vol. 26, Issue 23 https://doi.org/10.1175/JCLI-D-12-00566.1	journal	December 2013
Marine Ecosystem Dynamics and Biogeochemical Cycling in the Community Earth System Model [CESM1(BGC)]: Comparison of the 1990s with the 2090s under the RCP4.5 and RCP8.5 Scenarios Moore, J. Keith; Lindsay, Keith; Doney, Scott C. Journal of Climate, Vol. 26, Issue 23 https://doi.org/10.1175/JCLI‐D‐12‐00566.1	journal	December 2013
Constraining bubble dynamics and mixing with dissolved gases: Implications for productivity measurements by oxygen mass balance Hamme, Roberta C.; Emerson, Steven R. Journal of Marine Research, Vol. 64, Issue 1 https://doi.org/10.1357/002224006776412322	journal	January 2006
Net and gross oxygen production from O2/Ar, 17O/16O and 18O/16O ratios Luz, B.; Barkan, E. Aquatic Microbial Ecology, Vol. 56 https://doi.org/10.3354/ame01296	journal	September 2009
Large-scale variability of planktonic net community metabolism in the Atlantic Ocean: importance of temporal changes in oligotrophic subtropical waters González, N.; Anadón, R.; Marañón, E. Marine Ecology Progress Series, Vol. 233 https://doi.org/10.3354/meps233021	journal	January 2002
Bacteriochlorophyll a in the ocean: Is anoxygenic bacterial photosynthesis important? Goericke, Ralf Limnology and Oceanography, Vol. 47, Issue 1 https://doi.org/10.4319/lo.2002.47.1.0290	journal	January 2002
Seasonal and interannual variability in sources of nitrogen supporting export in the oligotrophic subtropical North Pacific Ocean Dore, John E.; Brum, Jennifer R.; Tupas, Luis M. Limnology and Oceanography, Vol. 47, Issue 6 https://doi.org/10.4319/lo.2002.47.6.1595	journal	November 2002
Global patterns in oceanic planktonic metabolism Regaudie-de-Gioux, Aurore; Duarte, Carlos M. Limnology and Oceanography, Vol. 58, Issue 3 https://doi.org/10.4319/lo.2013.58.3.0977	journal	May 2013
Historical (1850–2000) gridded anthropogenic and biomass burning emissions of reactive gases and aerosols: methodology and application Lamarque, J. -F.; Bond, T. C.; Eyring, V. Atmospheric Chemistry and Physics, Vol. 10, Issue 15 https://doi.org/10.5194/acp-10-7017-2010	journal	January 2010
Historical (1850–2000) gridded anthropogenic and biomass burning emissions of reactive gases and aerosols: methodology and application Lamarque, J. -F.; Bond, T. C.; Eyring, V. Atmospheric Chemistry and Physics, Vol. 10, Issue 15 https://doi.org/10.5194/acp‐10‐7017‐2010	journal	January 2010
Variable C : N : P stoichiometry of dissolved organic matter cycling in the Community Earth System Model Letscher, R. T.; Moore, J. K.; Teng, Y. -C. Biogeosciences, Vol. 12, Issue 1 https://doi.org/10.5194/bg-12-209-2015	journal	January 2015
Variable C : N : P stoichiometry of dissolved organic matter cycling in the Community Earth System Model Letscher, R. T.; Moore, J. K.; Teng, Y. -C. Biogeosciences, Vol. 12, Issue 1 https://doi.org/10.5194/bg‐12‐209‐2015	journal	January 2015

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54 ENVIRONMENTAL SCIENCES
58 GEOSCIENCES
autotrophic
heterotrophic
metabolic state
net community production
oligotrophic gyres

Modest net autotrophy in the oligotrophic ocean

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