Microbial iron limitation in the ocean's twilight zone.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Sep 2024
Historique:
received: 13 12 2023
accepted: 05 08 2024
medline: 26 9 2024
pubmed: 26 9 2024
entrez: 25 9 2024
Statut: ppublish

Résumé

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 biomass

Identifiants

pubmed: 39322731
doi: 10.1038/s41586-024-07905-z
pii: 10.1038/s41586-024-07905-z
doi:

Substances chimiques

Iron E1UOL152H7
Siderophores 0
Carbon 7440-44-0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

823-827

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Arrigo, K. R. Marine microorganisms and global nutrient cycles. Nature 437, 349–355 (2005).
pubmed: 16163345 doi: 10.1038/nature04159
Moore, C. M. et al. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 6, 701–710 (2013).
doi: 10.1038/ngeo1765
Browning, T. J. & Moore, C. M. Global analysis of ocean phytoplankton nutrient limitation reveals high prevalence of co-limitation. Nat. Commun. 14, 5014 (2023).
pubmed: 37591895 pmcid: 10435517 doi: 10.1038/s41467-023-40774-0
Buesseler, K. O. et al. Metrics that matter for assessing the ocean biological carbon pump. Proc. Natl Acad. Sci. USA 117, 9679–9687 (2020).
pubmed: 32253312 pmcid: 7211944 doi: 10.1073/pnas.1918114117
Buesseler, K. O. et al. Revisiting carbon flux through the ocean’s twilight zone. Science 316, 567–570 (2007).
pubmed: 17463282 doi: 10.1126/science.1137959
Baltar, F. et al. Specific effects of trace metals on marine heterotrophic microbial activity and diversity: key role of iron and zinc and hydrocarbon-degrading bacteria. Front. Microbiol. 9, 03190 (2018).
doi: 10.3389/fmicb.2018.03190
Bundy, R. M. et al. Distinct siderophores contribute to iron cycling in the mesopelagic at station ALOHA. Front. Mar. Sci. 5, 61 (2018).
doi: 10.3389/fmars.2018.00061
Mazzotta, M. G., McIlvin, M. R. & Saito, M. A. Characterization of the Fe metalloproteome of a ubiquitous marine heterotroph, Pseudoalteromonas (BB2-AT2): multiple bacterioferritin copies enable significant Fe storage. Metallomics 12, 654–667 (2020).
pubmed: 32301469 doi: 10.1039/d0mt00034e
Bagg, A. & Neilands, J. B. Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol. Rev. 51, 509–518 (1987).
pubmed: 2963952 pmcid: 373130 doi: 10.1128/mr.51.4.509-518.1987
Bressac, M. et al. Resupply of mesopelagic dissolved iron controlled by particulate iron composition. Nat. Geosci. 12, 995–1000 (2019).
doi: 10.1038/s41561-019-0476-6
Twining, B. S. et al. Differential remineralization of major and trace elements in sinking diatoms. Limnol. Oceanogr. 59, 689–704 (2014).
doi: 10.4319/lo.2014.59.3.0689
Bruland, K. W., Orians, K. J. & Cowen, J. P. Reactive trace metals in the stratified central North Pacific. Geochim. Cosmochim. Acta 58, 3171–3182 (1994).
doi: 10.1016/0016-7037(94)90044-2
Boyd, P. W., Ellwood, M. J., Tagliabue, A. & Twining, B. S. Biotic and abiotic retention, recycling and remineralization of metals in the ocean. Nat. Geosci. 10, 167–173 (2017).
doi: 10.1038/ngeo2876
Schlitzer, R. et al. The GEOTRACES Intermediate Data Product 2017. Chem. Geol. 493, 210–223 (2018).
doi: 10.1016/j.chemgeo.2018.05.040
Tortell, P. D., Maldonado, M. T. & Price, N. M. The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature 383, 330–332 (1996).
doi: 10.1038/383330a0
Fourquez, M. et al. Effects of iron limitation on growth and carbon metabolism in oceanic and coastal heterotrophic bacteria. Limnol. Oceanogr. 59, 349–360 (2014).
doi: 10.4319/lo.2014.59.2.0349
van den Berg, C. M. Evidence for organic complexation of iron in seawater. Mar. Chem. 50, 139–157 (1995).
doi: 10.1016/0304-4203(95)00032-M
Rue, E. L. & Bruland, K. W. 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. Mar. Chem. 50, 117–138 (1995).
doi: 10.1016/0304-4203(95)00031-L
Gledhill, M. & Buck, K. N. The organic complexation of iron in the marine environment: a review. Front. Microbiol. 3, 69 (2012).
pubmed: 22403574 pmcid: 3289268 doi: 10.3389/fmicb.2012.00069
Hassler, C. S., van den Berg, C. M. G. & Boyd, P. W. Toward a regional classification to provide a more inclusive examination of the ocean biogeochemistry of iron-binding ligands. Front. Mar. Sci. 4, 19 (2017).
doi: 10.3389/fmars.2017.00019
Sexton, D. J. & Schuster, M. Nutrient limitation determines the fitness of cheaters in bacterial siderophore cooperation. Nat. Commun. 8, 230 (2017).
pubmed: 28794499 pmcid: 5550491 doi: 10.1038/s41467-017-00222-2
Sijerčić, A. & Price, N. M. Hydroxamate siderophore secretion by Pseudoalteromonas haloplanktis during steady-state and transient growth under iron limitation. Mar. Ecol. Prog. Ser. 531, 105–120 (2015).
doi: 10.3354/meps11338
Gauglitz, J. M. et al. Dynamic proteome response of a marine Vibrio to a gradient of iron and ferrioxamine bioavailability. Mar. Chem. 229, 103913 (2021).
doi: 10.1016/j.marchem.2020.103913
Park, J. et al. Siderophore production and utilization by marine bacteria in the North Pacific Ocean. Limnol. Oceanogr. 68, 1636–1653 (2023).
doi: 10.1002/lno.12373
Martin, J. H. et al. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371, 123–129 (1994).
doi: 10.1038/371123a0
Martinez, J. S. et al. Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium. Proc. Natl Acad. Sci. USA 100, 3754–3759 (2003).
pubmed: 12651947 pmcid: 152994 doi: 10.1073/pnas.0637444100
Martinez, J. S. et al. Self-assembling amphiphilic siderophores from marine bacteria. Science 287, 1245–1247 (2000).
pubmed: 10678827 doi: 10.1126/science.287.5456.1245
Xu, G., Martinez, J. S., Groves, J. T. & Butler, A. Membrane affinity of the amphiphilic marinobactin siderophores. J. Am. Chem. Soc. 124, 13408–13415 (2002).
pubmed: 12418892 doi: 10.1021/ja026768w
Kramer, J., Özkaya, Ö. & Kümmerli, R. Bacterial siderophores in community and host interactions. Nat. Rev. Microbiol. 18, 152–163 (2020).
pubmed: 31748738 doi: 10.1038/s41579-019-0284-4
Saha, R., Saha, N., Donofrio, R. S. & Bestervelt, L. L. Microbial siderophores: a mini review. J. Basic Microbiol. 53, 303–317 (2012).
pubmed: 22733623 doi: 10.1002/jobm.201100552
Wilson, B. R., Bogdan, A. R., Miyazawa, M., Hashimoto, K. & Tsuji, Y. Siderophores in iron metabolism: from mechanism to therapy potential. Trends Mol. Med. 22, 1077–1090 (2016).
pubmed: 27825668 pmcid: 5135587 doi: 10.1016/j.molmed.2016.10.005
Schalk, I. J. & Guillon, L. Fate of ferrisiderophores after import across bacterial outer membranes: different iron release strategies are observed in the cytoplasm or periplasm depending on the siderophore pathways. Amino Acids 44, 1267–1277 (2013).
pubmed: 23443998 doi: 10.1007/s00726-013-1468-2
Greenwald, J. et al. Real time fluorescent resonance energy transfer visualization of ferric pyoverdine uptake in Pseudomonas aeruginosa: a role for ferrous iron. J. Biol. Chem. 282, 2987–2995 (2007).
pubmed: 17148441 doi: 10.1074/jbc.M609238200
Karl, D. M. & Church, M. J. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat. Rev. Microbiol. 12, 699–713 (2014).
pubmed: 25157695 doi: 10.1038/nrmicro3333
Hu, X. & Boyer, G. L. Siderophore-mediated aluminum uptake by Bacillus megaterium ATCC 19213. Appl. Environ. Microbiol. 62, 4044–4048 (1996).
pubmed: 16535439 pmcid: 1388977 doi: 10.1128/aem.62.11.4044-4048.1996
Giering, S. L. C. et al. Reconciliation of the carbon budget in the ocean’s twilight zone. Nature 507, 480–483 (2014).
pubmed: 24670767 doi: 10.1038/nature13123
Steinberg, D. K. et al. Bacterial vs. zooplankton control of sinking particle flux in the ocean’s twilight zone. Limnol. Oceanogr. 53, 1327–1338 (2008).
doi: 10.4319/lo.2008.53.4.1327
Pakulski, J. D. et al. Iron stimulation of Antarctic bacteria. Nature 383, 133–134 (1996).
doi: 10.1038/383133b0
Granger, J. & Price, N. M. The importance of siderophores in iron nutrition of heterotrophic marine bacteria. Limnol. Oceanogr. 44, 541–555 (1999).
doi: 10.4319/lo.1999.44.3.0541
Church, M. J., Hutchins, D. A. & Ducklow, H. W. Limitation of bacterial growth by dissolved organic matter and iron in the Southern Ocean. Appl. Environ. Microbiol. 66, 455–466 (2000).
pubmed: 10653704 pmcid: 91849 doi: 10.1128/AEM.66.2.455-466.2000
Mendonca, C. M. et al. Hierarchical routing in carbon metabolism favors iron-scavenging strategy in iron-deficient soil Pseudomonas species. Proc. Natl Acad. Sci. USA 117, 32358–32369 (2020).
pubmed: 33273114 pmcid: 7768705 doi: 10.1073/pnas.2016380117
Kirchman, D. L., Hoffman, K. A., Weaver, R. & Hutchins, D. A. Regulation of growth and energetics of a marine bacterium by nitrogen source and iron availability. Mar. Ecol. Prog. Ser. 250, 291–296 (2003).
doi: 10.3354/meps250291
Beier, S. et al. The transcriptional regulation of the glyoxylate cycle in SAR11 in response to iron fertilization in the Southern Ocean. Environ. Microbiol. Rep. 7, 427–434 (2015).
pubmed: 25625554 doi: 10.1111/1758-2229.12267
Kwon, E. Y., Primeau, F. & Sarmeento, J. L. The impact of remineralization depth on the air–sea carbon balance. Nat. Geosci. 2, 630–635 (2009).
doi: 10.1038/ngeo612
Fitzsimmons, J. N. et al. Daily to decadal variability of size-fractionated iron and iron-binding ligands at the Hawaii Ocean Time-series Station ALOHA. Geochim. Cosmochim. Acta 171, 303–324 (2015).
doi: 10.1016/j.gca.2015.08.012
Conway, T. M., Rosenberg, A. D., Adkins, J. F. & John, S. G. A new method for precise determination of iron, zinc and cadmium stable isotope ratios in seawater by double-spike mass spectrometry. Anal. Chim. Acta 793, 44–52 (2013).
pubmed: 23953205 doi: 10.1016/j.aca.2013.07.025
Sieber, M. et al. Isotopic fingerprinting of biogeochemical processes and iron sources in the iron-limited surface Southern Ocean. Earth Planet. Sci. Lett. 567, 116967 (2021).
doi: 10.1016/j.epsl.2021.116967
Middag, R. et al. Intercomparison of dissolved trace elements at the Bermuda Atlantic Time Series station. Mar. Chem. 177, 476–489 (2015).
doi: 10.1016/j.marchem.2015.06.014
Ellwood, M. J. et al. Distinct iron cycling in a Southern Ocean eddy. Nat. Commun. 11, 825 (2020).
pubmed: 32047154 pmcid: 7012851 doi: 10.1038/s41467-020-14464-0
Li, J. et al. Element-selective targeting of nutrient metabolites in environmental samples by inductively coupled plasma mass spectrometry and electrospray ionization mass spectrometry. Front. Mar. Sci. 8, 630494 (2021).
doi: 10.3389/fmars.2021.630494
Boiteau, R. M., Fitzsimmons, J. N., Repeta, D. J. & Boyle, E. A. Detection of iron ligands in seawater and marine cyanobacteria cultures by high-performance liquid chromatography–inductively coupled plasma-mass spectrometry. Anal. Chem. 85, 4357–4362 (2013).
pubmed: 23544623 doi: 10.1021/ac3034568
Boiteau, R. M. & Repeta, D. J. An extended siderophore suite from Synechococcus sp. PCC 7002 revealed by LC-ICPMS-ESIMS. Metallomics 7, 877–884 (2015).
pubmed: 25786191 doi: 10.1039/C5MT00005J
Chambers, M. C. et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 30, 918–920 (2012).
pubmed: 23051804 pmcid: 3471674 doi: 10.1038/nbt.2377
Baars, O., Morel, F. M. & Perlman, D. H. ChelomEx: isotope-assisted discovery of metal chelates in complex media using high-resolution LC-MS. Anal. Chem. 86, 11298–11305 (2014).
pubmed: 25333600 doi: 10.1021/ac503000e
Boiteau, R. M. Molecular Determination of Marine Iron Ligands by Mass Spectrometry. Thesis, Massachusetts Institute of Technology/Woods Hole Oceanographic Institution (2016).
Vraspir, J. M., Holt, P. D. & Butler, A. Identification of new members within suites of amphiphilic marine siderophores. BioMetals 24, 85–92 (2011).
pubmed: 20853137 doi: 10.1007/s10534-010-9378-1
Boiteau, R. M. et al. Siderophore-based microbial adaptations to iron scarcity across the eastern Pacific Ocean. Proc. Natl Acad. Sci. 113, 14237–14242 (2016).
pubmed: 27911777 pmcid: 5167167 doi: 10.1073/pnas.1608594113
Kem, M. P. & Butler, A. Acyl peptidic siderophores: structures, biosyntheses and post-assembly modifications. BioMetals 28, 445–459 (2015).
pubmed: 25677460 doi: 10.1007/s10534-015-9827-y
GEOTRACES Intermediate Data Product Group. The GEOTRACES Intermediate Data Product 2021 version 2 (IDP2021v2). NERC EDS British Oceanographic Data Centre NOC. https://doi.org/10.5285/ff46f034-f47c-05f9-e053-6c86abc0dc7e (2023).
Xiang, Y. & Lam, P. J. Size-fractionated compositions of marine suspended particles in the Western Arctic Ocean: lateral and vertical sources. J. Geophys. Res. Oceans 125, e2020JC016144 (2020).
doi: 10.1029/2020JC016144

Auteurs

Jingxuan Li (J)

Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.
Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.

Lydia Babcock-Adams (L)

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

Rene M Boiteau (RM)

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

Matthew R McIlvin (MR)

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

Lauren E Manck (LE)

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

Matthias Sieber (M)

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

Nathan T Lanning (NT)

Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.
Department of Oceanography, Texas A&M University, College Station, TX, USA.

Randelle M Bundy (RM)

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

Xiaopeng Bian (X)

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

Iulia-Mădălina Ștreangă (IM)

Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.
Department of Earth, Atmospheric, and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA.

Benjamin N Granzow (BN)

Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.
Geosciences Research Division, Scripps Institution of Oceanography, La Jolla, CA, USA.

Matthew J Church (MJ)

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

Jessica N Fitzsimmons (JN)

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

Seth G John (SG)

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

Tim M Conway (TM)

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

Daniel J Repeta (DJ)

Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA. drepeta@whoi.edu.

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Classifications MeSH