Light-driven integration of diazotroph-derived nitrogen in euphotic nitrogen cycle.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
24 Oct 2024
24 Oct 2024
Historique:
received:
16
05
2024
accepted:
30
09
2024
medline:
25
10
2024
pubmed:
25
10
2024
entrez:
25
10
2024
Statut:
epublish
Résumé
The bioavailable nitrogen fixed by diazotrophs is critical for sustaining productivity in the oligotrophic ocean. Despite this, understanding how diazotroph-derived nitrogen integrates into the nitrogen cycle within the euphotic zone remains unknown. Here, we investigated nitrogen fixation rates in the particulate and dissolved fractions within the euphotic zone of the North Pacific Subtropical Gyre. Our findings reveal the proportion of nitrogen fixation rates in the dissolved fraction increases with depth. Light manipulation experiments uncover that reduced light levels can stimulate the net release of diazotroph-derived nitrogen, aligning with our depth-related observations. Furthermore, we identify two distinct transfer pathways vertically associated with light-driven ecological niches. Specifically, the released diazotroph-derived nitrogen is transferred to non-diazotrophic plankton in the upper layers. Meanwhile, in the lower layers, it contributes to the nitrification process. Our results underscore the high bioavailability of diazotroph-derived nitrogen and its rapid integration into the nitrogen cycle through multiple pathways within the well-lit ocean.
Identifiants
pubmed: 39448610
doi: 10.1038/s41467-024-53067-x
pii: 10.1038/s41467-024-53067-x
doi:
Substances chimiques
Nitrogen
N762921K75
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9193Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 92258302
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 41721005
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 92058204
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 42106048
Organisme : Simons Foundation
ID : 675459
Informations de copyright
© 2024. The Author(s).
Références
Zehr, J. P. & Capone, D. G. Changing perspectives in marine nitrogen fixation. Science 368, eaay9514 (2020).
pubmed: 32409447
doi: 10.1126/science.aay9514
Böttjer, D. et al. Temporal variability of nitrogen fixation and particulate nitrogen export at station ALOHA. Limnol. Oceanogr. 62, 200–216 (2017).
doi: 10.1002/lno.10386
Mills, M. M. & Arrigo, K. R. The magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton. Nat. Geosci. 3, 412–416 (2010).
doi: 10.1038/ngeo856
Mulholland, M. R. The fate of nitrogen fixed by diazotrophs in the ocean. Biogeosciences 4, 37–51 (2007).
doi: 10.5194/bg-4-37-2007
Glibert, P. M. & Bronk, D. A. Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 60, 3996–4000 (1994).
pubmed: 16349432
pmcid: 201927
doi: 10.1128/aem.60.11.3996-4000.1994
Carpenter, E. J., & Capone, D. G. (Eds.). Marine pelagic cyanobacteria: trichodesmium and other diazotrophs 362, Springer Science & Business Media (1992).
Glibert, P. M., & O’neil, J. M. Dissolved organic nitrogen release and amino acid oxidase activity by Trichodesmium spp. Bull. Inst. océanogr. 265–272 (1999).
Berman-Frank, I., Bidle, K. D., Haramaty, L. & Falkowski, P. G. The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol. Oceanogr. 49, 997–1005 (2004).
doi: 10.4319/lo.2004.49.4.0997
Lu, Y. et al. Effect of light on N
doi: 10.5194/bg-15-1-2018
Hewson, I., Govil, S. R., Capone, D. G., Carpenter, E. J. & Fuhrman, J. A. Evidence of Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean. Aquat. Microb. Ecol. 36, 1–8 (2004).
doi: 10.3354/ame036001
O’Neil, J. M. Grazer interactions with nitrogen-fixing marine Cyanobacteria: adaptation for N-acquisition? Bull. Inst. océanogr. 293–318 (1999).
Fawcett, S. E., Lomas, M. W., Casey, J. R., Ward, B. B. & Sigman, D. M. Assimilation of upwelled nitrate by small eukaryotes in the Sargasso Sea. Nat. Geosci. 4, 717–722 (2011).
doi: 10.1038/ngeo1265
Hunt, B. P. et al. Contribution and pathways of diazotroph-derived nitrogen to zooplankton during the VAHINE mesocosm experiment in the oligotrophic New Caledonia lagoon. Biogeosciences 13, 3131–3145 (2016).
doi: 10.5194/bg-13-3131-2016
Caffin, M., Berthelot, H., Cornet-Barthaux, V., Barani, A. & Bonnet, S. Transfer of diazotroph-derived nitrogen to the planktonic food web across gradients of N
doi: 10.5194/bg-15-3795-2018
Mulholland, M. R., Heil, C. A., Bronk, D. A., O’Neil, J. M. & Bernhardt, P. Does nitrogen regeneration from the N
Bonnet, S. et al. Diazotroph derived nitrogen supports diatom growth in the South West Pacific: a quantitative study using nanoSIMS. Limnol. Oceanogr. 61, 1549–1562 (2016).
doi: 10.1002/lno.10300
Bonnet, S. et al. Dynamics of N
doi: 10.5194/bg-13-2653-2016
Shao, Z. et al. Global oceanic diazotroph database version 2 and elevated estimate of global N
Berthelot, H., Benavides, M., Moisander, P. H., Grosso, O. & Bonnet, S. High‐nitrogen fixation rates in the particulate and dissolved pools in the Western Tropical Pacific (Solomon and Bismarck Seas). Geophys. Res. Lett. 44, 8414–8423 (2017).
doi: 10.1002/2017GL073856
Wan, X. S. et al. Ambient nitrate switches the ammonium consumption pathway in the euphotic ocean. Nat. Commun. 9, 915 (2018).
pubmed: 29500422
pmcid: 5834513
doi: 10.1038/s41467-018-03363-0
Lu, Y. et al. Biogeography of N
doi: 10.1029/2018JC014781
Shiozaki, T. et al. Basin scale variability of active diazotrophs and nitrogen fixation in the North Pacific, from the tropics to the subarctic Bering Sea. Glob. Biogeochem. Cycles 31, 996–1009 (2017).
doi: 10.1002/2017GB005681
Wen, Z. et al. Nutrient regulation of biological nitrogen fixation across the tropical western North Pacific. Sci. Adv. 8, eabl7564 (2022).
pubmed: 35119922
pmcid: 8816331
doi: 10.1126/sciadv.abl7564
Gradoville, M. R. et al. Light and depth dependency of nitrogen fixation by the non‐photosynthetic, symbiotic cyanobacterium UCYN‐A. Environ. Microbiol. 23, 4518–4531 (2021).
pubmed: 34227720
pmcid: 9291983
doi: 10.1111/1462-2920.15645
Garcia, N. S., Fu, F.-X. & Hutchins, D. A. Colimitation of the unicellular photosynthetic diazotroph Crocosphaera watsonii by phosphorus, light, and carbon dioxide. Limnol. Oceanogr. 58, 1501–1512 (2013).
doi: 10.4319/lo.2013.58.4.1501
Lomas, M. W., Rumbley, C. J. & Glibert, P. M. Ammonium release by nitrogen sufficient diatoms in response to rapid increases in irradiance. J. Plankton Res. 22, 2351–2366 (2000).
doi: 10.1093/plankt/22.12.2351
Hansell, D. A., & Carlson, C. A. (Eds.). Biogeochemistry of marine dissolved organic matter. (Academic Press, 2014).
Yu-Fang, T., Fei-Jen, L., Chiang, K. P., Kao, S. J. & Shiah, F. K. Potential impacts of N
doi: 10.3319/TAO.2005.16.2.361(Oc)
Xu, M. N. et al. Coupled effect of substrate and light on assimilation and oxidation of regenerated nitrogen in the euphotic ocean. Limnol. Oceanogr. 64, 1270–1283 (2019).
doi: 10.1002/lno.11114
Deng, L., Cheung, S., Xu, Z., Liu, K. & Liu, H. Microzooplankton grazing exerts a strong top‐down control on unicellular cyanobacterial diazotrophs. J. Geophys. Res. Biogeosci. 128, e2023JG007824 (2023).
doi: 10.1029/2023JG007824
Fuhrman, J. Close coupling between release and uptake of dissolved free amino acids in seawater studied by an isotope dilution approach. Mar. Ecol. Prog. Ser. 37, 45–52 (1987).
doi: 10.3354/meps037045
Adam, B. et al. N
pubmed: 26262817
doi: 10.1038/ismej.2015.126
Bronk, D. A., Glibert, P. M., Malone, T. C., Banahan, S. & Sahlsten, E. Inorganic and organic nitrogen cycling in Chesapeake Bay: autotrophic versus heterotrophic processes and relationships to carbon flux. Aquat. Microb. Ecol. 15, 177–189 (1998).
doi: 10.3354/ame015177
Moore, C. M. et al. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 6, 701–710 (2013).
doi: 10.1038/ngeo1765
Galloway, J. N. et al. Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153–226 (2004).
doi: 10.1007/s10533-004-0370-0
Codispoti, L. A. et al. The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene? Sci. Mar. 65, 85–105 (2001).
doi: 10.3989/scimar.2001.65s285
Gruber, N. The dynamics of the marine nitrogen cycle and its influence on atmospheric CO
Yool, A., Martin, A. P., Fernández, C. & Clark, D. R. The significance of nitrification for oceanic new production. Nature 447, 999–1002 (2007).
pubmed: 17581584
doi: 10.1038/nature05885
Liu, L. et al. Reduced nitrite accumulation at the primary nitrite maximum in the cyclonic eddies in the western North Pacific subtropical gyre. Sci. Adv. 9, eade2078 (2023).
pubmed: 37585519
pmcid: 10431711
doi: 10.1126/sciadv.ade2078
Wan, X. S. et al. Epipelagic nitrous oxide production offsets carbon sequestration by the biological pump. Nat. Geosci. 16, 29–36 (2023).
doi: 10.1038/s41561-022-01090-2
Kara, A. B., Rochford, P. A. & Hurlburt, H. E. An optimal definition for ocean mixed layer depth. J. Geophys. Res. Oceans 105, 16803–16821 (2000).
doi: 10.1029/2000JC900072
Siegel, D. A., Michaels, A. F., Sorensen, J. C., O’Brien, M. C. & Hammer, M. A. Seasonal variability of light availability and utilization in the Sargasso Sea. J. Geophys. Res. Oceans 100, 8695–8713 (1995).
doi: 10.1029/95JC00447
White, A. E. et al. A critical review of the
doi: 10.1002/lom3.10353
Shen, H., et al. Physical optima for nitrogen fixation in cyclonic eddies in the Subtropical Northwestern Pacific. Prog. Oceanogr. 226, 103298 (2024).
Knapp, A. N., Sigman, D. M., & Lipschultz, F. N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda Atlantic time‐series Study site. Glob. Biogeochem. Cycles 19 (2005).
Braman, R. S. & Hendrix, S. A. Nanogram nitrite and nitrate determination in environmental and biological materials by vanadium (III) reduction with chemiluminescence detection. Anal. Chem. 61, 2715–2718 (1989).
pubmed: 2619057
doi: 10.1021/ac00199a007
Casciotti, K. L., Sigman, D. M., Hastings, M. G., Böhlke, J. K. & Hilkert, A. Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal. Chem. 74, 4905–4912 (2002).
pubmed: 12380811
doi: 10.1021/ac020113w
Sigman, D. M. et al. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal. Chem. 73, 4145–4153 (2001).
pubmed: 11569803
doi: 10.1021/ac010088e
Montoya, J. P., Voss, M., Kahler, P. & Capone, D. G. A simple, high-precision, high-sensitivity tracer assay for N
pubmed: 16535283
pmcid: 1388808
doi: 10.1128/aem.62.3.986-993.1996
Platt, T. G. C. L., Gallegos, C. L., & Harrison, W. G. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38 (1980).
Chen, M. et al. Biogeographic drivers of diazotrophs in the western Pacific Ocean. Limnol. Oceanogr. 64, 1403–1421 (2019).
doi: 10.1002/lno.11123
Hama, T. et al. Measurement of photosynthetic production of a marine phytoplankton population using a stable
doi: 10.1007/BF00396282
Han, A. et al. Nutrient dynamics and biological consumption in a large continental shelf system under the influence of both a river plume and coastal upwelling. Limnol. Oceanogr. 57, 486–502 (2012).
doi: 10.4319/lo.2012.57.2.0486
Du, C. et al. Impact of the Kuroshio intrusion on the nutrient inventory in the upper northern South China Sea: insights from an isopycnal mixing model. Biogeosciences 10, 6419–6432 (2013).
doi: 10.5194/bg-10-6419-2013
Du, C., Liu, Z., Kao, S. J. & Dai, M. Diapycnal fluxes of nutrients in an oligotrophic oceanic regime: the South China Sea. Geophys. Res. Lett. 44, 11–510 (2017).
doi: 10.1002/2017GL074921