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Microbial iron limitation in the ocean’s twilight zone

Nature volume 633, pages 823–827 (2024)Cite this article

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Abstract

Primary production in the sunlit surface ocean is regulated by the supply of key nutrients, primarily nitrate, phosphate and iron (Fe), required by phytoplankton to fix carbon dioxide into biomass1,2,3. Below the surface ocean, remineralization of sinking organic matter rapidly regenerates nutrients, and microbial metabolism in the upper mesopelagic ‘twilight zone’ (200–500 m) is thought to be limited by the delivery of labile organic carbon4,5. However, few studies have examined the role of nutrients in shaping microbial production in the mesopelagic6,7,8. Here we report the distribution and uptake of siderophores, biomarkers for microbial Fe deficiency9 across a meridional section of the eastern Pacific Ocean. Siderophore concentrations are high not only in chronically Fe-limited surface waters but also in the twilight zone underlying the North and South Pacific subtropical gyres, two key ecosystems for the marine carbon cycle. Our findings suggest that bacterial Fe deficiency owing to low Fe availability is probably characteristic of the twilight zone in several large ocean basins, greatly expanding the region of the marine water column in which nutrients limit microbial metabolism, with potential implications for ocean carbon storage.

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Fig. 1: High siderophore concentrations in the mesopelagic of the eastern Pacific Ocean.
Fig. 2: Nutrient regulation of siderophore distribution.
Fig. 3: Fe–siderophore cycling in the mesopelagic ocean.
Fig. 4: Cycling of siderophores for Fe in the twilight zone of the North Pacific Subtropical Gyre.

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Data availability

Siderophore concentration data for the GP15 transect are publicly available through the BCODMO data archive (https://www.bco-dmo.org/dataset/875210 and https://www.bco-dmo.org/dataset/929884). Dissolved iron data for the GP15 transect have been deposited in BCODMO (https://www.bco-dmo.org/dataset/883862 and https://www.bco-dmo.org/dataset/884673). Nitrate data have been deposited in BCODMO (https://www.bco-dmo.org/dataset/777951 and https://www.bco-dmo.org/dataset/824867). The nitrate data in Fig. 3 are from the Hawaii Ocean Time-series (HOT) data archive at the University of Hawai’i at Manoa (https://hahana.soest.hawaii.edu/hot/methods/llnuts.html). Siderophore concentration data for the uptake experiment are provided at https://zenodo.org/records/12206828. The LC-ESIMS data for Extended Data Figs. 2 and 3 and Extended Data Table 1 are available at MassIVE (https://massive.ucsd.edu/ProteoSAFe/dataset.jsp?task=7439be618f5949ecb1c2eac35978dba4).

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Acknowledgements

We thank P. Lam, K. Casciotti, G. Cutter, B. Summers and L. Jensen for their organization, assistance and support of the GP15 expedition. P. Morton provided assistance for the inductively coupled plasma mass spectrometry analyses at Texas A&M University. We also thank T. Burrell, R. Tabata, B. Brenes, D. Karl, A. White, P. Kong and M. Seixas for their support and assistance of the PARAGON 2022 cruise on the R/V Kilo Moana. Funding for this work was provided by National Science Foundation Chemical Oceanography Program (NSF awards OCE-1736280 and OCE-2045223 to D.J.R.; OCE-1737167 to J.N.F.; OCE-1737136 to T.M.C.; and OCE-1736896 to S.G.J.). Support was also provided for the Simons Collaboration on Ocean Processes and Ecology programme (SCOPE awards 721227 to D.J.R. and 721221 to M.J.C.), Simons Foundation Early Career Investigator Awards in Marine Microbial Ecology and Evolution (Life Sciences awards 621513 to R.M.Bo and 618401 to R.M.Bu.) and a Simons Foundation Postdoctoral Fellowship in Marine Ecology (award 729162 to L.E.M.).

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Author notes

  1. These authors contributed equally: Jingxuan Li, Lydia Babcock-Adams

Authors and Affiliations

  1. Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA

    Jingxuan Li, Matthew R. McIlvin, Iulia-Mădălina Ștreangă, Benjamin N. Granzow & Daniel J. Repeta

  2. Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA

    Jingxuan Li, Nathan T. Lanning & Iulia-Mădălina Ștreangă

  3. Ion Cyclotron Resonance Program, National High Magnetic Field Laboratory, Florida State University, Tallahassee, FL, USA

    Lydia Babcock-Adams

  4. Department of Chemistry, University of Minnesota, Minneapolis, MN, USA

    Rene M. Boiteau

  5. Flathead Lake Biological Station, University of Montana, Polson, MT, USA

    Lauren E. Manck & Matthew J. Church

  6. College of Marine Science, University of South Florida, St Petersburg, FL, USA

    Matthias Sieber & Tim M. Conway

  7. Department of Oceanography, Texas A&M University, College Station, TX, USA

    Nathan T. Lanning & Jessica N. Fitzsimmons

  8. School of Oceanography, University of Washington, Seattle, WA, USA

    Randelle M. Bundy

  9. Department of Earth Sciences, University of Southern California, Los Angeles, CA, USA

    Xiaopeng Bian & Seth G. John

  10. Geosciences Research Division, Scripps Institution of Oceanography, La Jolla, CA, USA

    Benjamin N. Granzow

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  1. Jingxuan Li
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Contributions

J.L., L.B.-A. and D.J.R. designed the project. J.L. and L.B.-A. collected and processed the GP15 samples. J.L., L.B.-A. and M.R.M. measured and characterized siderophores in the GP15 and PARAGON 2022 samples. D.J.R., J.N.F., R.M.Bo. and R.M.Bu. developed the liquid chromatography–mass spectrometry methods and data interrogation algorithms and purified marinobactins for the PARAGON 2022 experiments. J.L., L.E.M., I.-M.S., B.N.G. and M.J.C. conducted the siderophore uptake experiments during the PARAGON 2022 cruise. M.S., N.T.L., X.B., T.M.C., J.N.F. and S.G.J. measured dissolved iron in the GP15 samples. J.L. and D.J.R. performed the data analysis and wrote the first draft of the paper. All authors contributed to writing the manuscript.

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Correspondence to Daniel J. Repeta.

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Extended data figures and tables

Extended Data Fig. 1 Molecular structures of representative marinobactins and amphibactins identified in GP15 samples.

Amphibactins and marinobactins are distinguished by the number and type of amino acids in the Fe-complexing peptide head group. Each family of siderophores has several homologues that differ in the number of CH2 groups and unsaturations in the fatty acid side chain.

Extended Data Fig. 2 Characterization of siderophores in GP15 samples.

a, The 56Fe chromatogram by LC-ICP-MS for sample at station 16, 400 m. b–e, Extracted ion chromatograms by LC-ESIMS from the same sample. Blue traces correspond to the 56Fe–siderophore [M + H]+ isotopologue and red traces correspond to the less abundant 54Fe–siderophore [M + H]+ isotopologue. The intensity of the 54Fe isotopologue has been scaled by the 56Fe/54Fe crustal abundance ratio of 15.7. Peaks were assigned as 56Fe–marinobactin A (m/z 985.401) (b), 56Fe–marinobactin B (m/z 1,011.416) (c), 56Fe–marinobactin C (m/z 1,013.432) (d) and 56Fe–marinobactin D (m/z 1,039.452) (e).

Extended Data Fig. 3 Validation of the 57Fe–siderophore amendment.

57Fe (dark blue trace) and 56Fe (light blue trace) chromatograms of amphibactin (a) and marinobactin (b) mixtures used for the siderophore uptake experiment. c, Extracted ion chromatograms for 57Fe–amphibactins in the amphibactin stock solution. Peaks were assigned as: A, 57Fe–amphibactin C10:0 (m/z 830.353); B, 57Fe–amphibactin C12:1 (m/z 856.368); C, 57Fe–amphibactin T (m/z 858.384); and D, 57Fe–amphibactin S (m/z 884.400). The peak with an m/z of 900.394 also represents an 57Fe–amphibactin but does not contribute to the main peaks in Fig. 4. d, Extracted ion chromatograms for 57Fe–marinobactins in the marinobactin stock solution. Peaks were assigned as: A, 57Fe–marinobactin A (m/z 986.406); B, 57Fe–marinobactin B (m/z 1,012.420); C, 57Fe–marinobactin C (m/z 1,014.437); and D, 57Fe–marinobactin D (m/z 1,040.452).

Extended Data Fig. 4 Sectional plots of nitrate:DFe ratio between the surface and at 500 m in different ocean basins.

a, GEOTRACES GP19 section in the South Pacific Ocean along 170° W. b, GEOTRACES GP16 section in the equatorial Pacific Ocean along 10–15° S. c, GEOTRACES GN01 section in the Arctic Ocean along 140° W–180° E. d, GEOTRACES GA03 section in the North Atlantic Ocean along 15–40° N. e, GEOTRACES GI04 section in the Indian Ocean along 40–85° E. f, GEOTRACES GA10 section in the South Atlantic Ocean along 35–40° S. The data were extracted from GEOTRACES Intermediate Data Product 2017 (ref. 14) and 2021 (ref. 59).

Extended Data Fig. 5 Sectional plots of DFe concentration between the surface and at 500 m in different ocean basins.

a, GEOTRACES GP19 section in the South Pacific Ocean along 170° W. b, GEOTRACES GP16 section in the equatorial Pacific Ocean along 10–15° S. c, GEOTRACES GN01 section in the Arctic Ocean along 140° W–180° E. d, GEOTRACES GA03 section in the North Atlantic Ocean along 15–40° N. e, GEOTRACES GI04 section in the Indian Ocean along 40–85° E. f, GEOTRACES GA10 section in the South Atlantic Ocean along 35–40° S. The data were extracted from GEOTRACES Intermediate Data Product 2017 (ref. 14) and 2021 (ref. 59).

Extended Data Fig. 6 Sectional plots of nitrate concentration between the surface and at 500 m in different ocean basins.

a, GEOTRACES GP19 section in the South Pacific Ocean along 170° W. b, GEOTRACES GP16 section in the equatorial Pacific Ocean along 10–15° S. c, GEOTRACES GN01 section in the Arctic Ocean along 140° W–180° E. d, GEOTRACES GA03 section in the North Atlantic Ocean along 15–40° N. e, GEOTRACES GI04 section in the Indian Ocean along 40–85° E. f, GEOTRACES GA10 section in the South Atlantic Ocean along 35–40° S. The data were extracted from GEOTRACES Intermediate Data Product 2017 (ref. 14) and 2021 (ref. 59).

Extended Data Table 1 The concentration of siderophores in the particulate samples paired with dissolved samples of the closest depth collected at that station
Full size table
Extended Data Table 2 Concentrations of 57Fe-siderophores (57Fe-S) and 27Al-siderophores (27Al-S) in seawater with depth after five days of incubation
Full size table
Extended Data Table 3 Total siderophore concentrations for peaks A-D (Fig. 4) after five days of incubation
Full size table

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Li, J., Babcock-Adams, L., Boiteau, R.M. et al. Microbial iron limitation in the ocean’s twilight zone. Nature 633, 823–827 (2024). https://doi.org/10.1038/s41586-024-07905-z

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