CoChat
Sign Up
Cited by 45Marine Plankton and BiogeochemistryMetalloenzymes and iron-sulfur proteinsAquatic Ecosystems and Phytoplankton Dynamics

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Co-occurrence of Fe and P stress in natural populations of the marine diazotroph Trichodesmium

Open access
Held, Noelle A., Webb, Eric A., McIlvin, Matthew M., Hutchins, David A., Cohen, Natalie R., Moran, Dawn M., Kunde, Korinna, Lohan, Maeve C., Mahaffey, Claire, Woodward, E. Malcolm S., Saito, Mak A.·2020·Biogeosciences
DOI 10.5194/bg-17-2537-2020

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

Trichodesmium is a globally important marine microbe that provides fixed nitrogen (N) to otherwise N-limited ecosystems. In nature, nitrogen fixation is likely regulated by iron or phosphate availability, but the extent and interaction of these controls are unclear. From metaproteomics analyses using established protein biomarkers for nutrient stress, we found that iron–phosphate co-stress is the norm rather than the exception for Trichodesmium colonies in the North Atlantic Ocean. Counterintuitively, the nitrogenase enzyme was more abundant under co-stress as opposed to single nutrient stress. This is consistent with the idea that Trichodesmium has a specific physiological state during nutrient co-stress. Organic nitrogen uptake was observed and occurred simultaneously with nitrogen fixation. The quantification of the phosphate ABC transporter PstA combined with a cellular model of nutrient uptake suggested that Trichodesmium is generally confronted by the biophysical limits of membrane space and diffusion rates for iron and phosphate acquisition in the field. Colony formation may benefit nutrient acquisition from particulate and organic sources, alleviating these pressures. The results highlight that to predict the behavior of Trichodesmium , both Fe and P stress must be evaluated simultaneously.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.5194/bg-17-2537-2020

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 72

  1. Basu, S. and Shaked, Y.: Mineral iron utilization by natural and cultured Trichodesmium and associated bacteria, Limnol. Oceanogr., 63, 2307–2320, 10.1002/lno.10939, 2018. · DOI
  2. Basu, S., Gledhill, M., de Beer, D., Matondkar, S. G. P., and Shaked, Y.: Colonies of marine cyanobacteria Trichodesmium interact with associated bacteria to acquire iron from dust, Communications Biology, 2, 1–8, 10.1038/s42003-019-0534-z, 2019. · DOI
  3. Bergman, B., Sandh, G., Lin, S., Larsson, J., and Carpenter, E. J.: Trichodesmium – a widespread marine cyanobacterium with unusual nitrogen fixation properties, FEMS Microbiol. Rev., 37, 286–302, 10.1111/j.1574-6976.2012.00352.x, 2013. · DOI
  4. Berman-Frank, I., Cullen, J. T., Shaked, Y., Sherrell, R. M., and Falkowski, P. G.: Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium, Limnol. Oceanogr., 46, 1249–1260, 10.4319/lo.2001.46.6.1249, 2001. · DOI
  5. Capone, D. G., Zehr, J. P., Paerl, H. W., Bergman, B., and Carpenter, E. J.: Trichodesmium, a globally significant marine cyanobacterium, Science, 276, 1221–1229, 10.1126/science.276.5316.1221, 1997. · DOI
  6. Carpenter, E. J. and Romans, K.: Major Role of the Cyanobacterium Trichodesmium in Nutrient Cycling in the North Atlantic Ocean, Science, 254, 1989–1992, 1991. · DOI
  7. Carpenter, E. J., Bergman, B., Dawson, R., Siddiqui, P. J., Söderbäck, E., and Capone, D. G.: Glutamine synthetase and nitrogen cycling in colonies of the marine diazotrophic cyanobacteria Trichodesmium spp., Appl. Environ. Microb., 58, 3122–3129, 1992. · DOI
  8. Chappell, P. D. and Webb, E. A.: A molecular assessment of the iron stress response in the two phylogenetic clades of Trichodesmium, Environ. Microbiol., 12, 13–27, 10.1111/j.1462-2920.2009.02026.x, 2010. · DOI
  9. Chappell, P. D., Moffett, J. W., Hynes, A. M., and Webb, E. A.: Molecular evidence of iron limitation and availability in the global diazotroph Trichodesmium, ISME J., 6, 1728–1739, 10.1038/ismej.2012.13, 2012. · DOI
  10. Chisholm, S. W.: Phytoplankton Size, in: Primary Productivity and Biogeochemical Cycles in the Sea, edited by: Falkowski, P. G., Woodhead, A. D., and Vivirito, K., Springer, Boston, USA, 213–237, 10.1007/978-1-4899-0762-2_12, 1992. · DOI
  11. Coles, V. J., Hood, R. R., Pascual, M., and Capone, D. G.: Modeling the impact of Trichodesmium and nitrogen fixation in the Atlantic ocean, J. Geophys. Res.-Oceans, 109, 1–17, 10.1029/2002JC001754, 2004. · DOI
  12. Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N., and Dunne, J. P.: Spatial coupling of nitrogen inputs and losses in the ocean, Nature, 445, 163–167, 10.1038/nature05392, 2007. · DOI
  13. Dyhrman, S. T., Chappell, P. D., Haley, S. T., Moffett, J. W., Orchard, E. D., Waterbury, J. B., and Webb, E. A.: Phosphonate utilization by the globally important marine diazotroph Trichodesmium, Nature, 439, 68–71, 10.1038/nature04203, 2006. · DOI
  14. Eichner, M., Thoms, S., Rost, B., Mohr, W., Ahmerkamp, S., Ploug, H., Kuypers, M. M. M., and de Beer, D.: N2 fixation in free-floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments, New Phytol., 222, 852–863, 10.1111/nph.15621, 2019. · DOI
  15. Eng, J. K., Fischer, B., Grossmann, J., and MacCoss, M. J.: A fast SEQUEST cross correlation algorithm, Journal of Proteome Research, 7(10), 4598–4602, 10.1021/pr800420s, 2008. · DOI
  16. Flores, E. and Herrero, A.: Nitrogen assimilation and nitrogen control in cyanobacteria, Biochem. Soc. T., 33, 164–167, 10.1042/BST0330164, 2005. · DOI
  17. Forchhammer, K. and de Marsac, N. T.: The P(II) protein in the cyanobacterium Synechococcus sp. strain PCC 7942 is modified by serine phosphorylation and signals the cellular N-status, J. Bacteriol., 176, 84–91, 1994. · DOI
  18. Frischkorn, K. R., Krupke, A., Guieu, C., Louis, J., Rouco, M., Salazar Estrada, A. E., Van Mooy, B. A. S., and Dyhrman, S. T.: Trichodesmium physiological ecology and phosphate reduction in the western tropical South Pacific, Biogeosciences, 15, 5761–5778, 10.5194/bg-15-5761-2018, 2018. · DOI
  19. Froelich, P. N., Bender, M. L., Luedtke, N. A., Heath, G. R., and DeVries, T.: The Marine Phosphorus Cycle, Am. J. Sci., 282, 464–511, 1982. · DOI
  20. Fu, Q., Chen, Z., Zhang, S., Parker, S. J., Fu, Z., Tin, A., Liu, X., and Van Eyk, J. E.: Multiple and Selective Reaction Monitoring Using Triple Quadrupole Mass Spectrometer: Preclinical Large Cohort Analysis, in: Quantitative Proteomics by Mass Spectrometry, edited by: Sechi, S., Springer, New York, USA, 249–264, 10.1007/978-1-4939-3524-6_15, 2016. · DOI
  21. Garcia, N. S., Fu, F., Sedwick, P. N., and Hutchins, D. A.: Iron deficiency increases growth and nitrogen-fixation rates of phosphorus-deficient marine cyanobacteria, ISME J., 9, 238–245, 10.1038/ismej.2014.104, 2015. · DOI
  22. Held, N. A. and Saito, M. A.: Trichodesmium field metaproteomes, PRIDE, 10.6019/PXD016225, 2019. · DOI
  23. Held, N. A. and Saito, M. A.: Trichodesmium sample provenance from samples collected in North Atlantic surface waters, station BATS, and station ALOHA between 2000 and 2018, Biological and Chemical Oceanography Data Management Office (BCO-DMO), Dataset version 2020-01-10, 10.26008/1912/bco-dmo.787093.1, 2020a. · DOI
  24. Held, N. A. and Saito, M. A.: Metaproteomes of Trichodesmium from samples collected in North Atlantic surface waters, station BATS, and station ALOHA between 2000 and 2018, Biological and Chemical Oceanography Data Management Office (BCO-DMO), Dataset version 2020-01-10, 10.26008/1912/bco-dmo.787078.1, 2020b. · DOI
  25. Held, N. A. and Saito, M. A.: Net tow metaproteome of Trichodesmium species mapped to a Trichodesmium metagenome plus cyanoGEBA species genomes in units of normalized protein spectral counts from samples collected in the Atlantic and Pacific Ocean between 2000 and 2018, Biological and Chemical Oceanography Data Management Office (BCO-DMO), Dataset version 2020-04-30, 10.26008/1912/bco-dmo.787147.1, 2020c. · DOI
  26. Held, N. A. and Saito, M. A.: Net tow metaproteoome of Trichodesmium species mapped to a Trichodesmium metagenome plus cyanoGEBA species genomes in units of normalized peptide spectral counts from samples collected in the Atlantic and Pacific Ocean between 2000 and 2018, Biological and Chemical Oceanography Data Management Office (BCO-DMO), Dataset version 2020-04-30, 10.26008/1912/bco-dmo.787168.1, 2020d. · DOI
  27. Held, N. A. and Saito, M. A.: FASTA file of sequences in Trichodesmium field metaproteomes mapped to a Trichodesmium metagenome plus cyanoGEBA species genomes from samples collected in the Atlantic and Pacific Ocean between 2000 and 2018, Biological and Chemical Oceanography Data Management Office (BCO-DMO), Dataset version 2020-01-14, 10.26008/1912/bco-dmo.787181.1, 2020e. · DOI
  28. Held, N. A., McIlvin, M. R., Moran, D. M., Laub, M. T., and Saito, M. A.: Unique Patterns and Biogeochemical Relevance of Two-Component Sensing in Marine Bacteria, MSystems, 4, e00317-18, 10.1128/mSystems.00317-18, 2019. · DOI
  29. Hudson, R. J. and Morel, F. M. M.: Trace metal transport by marine microorganisms: implications of metal coordination kinetics, Deep-Sea Res. Pt. I, 40, 129–150, 1992. · DOI
  30. Hynes, A. M., Chappell, P. D., Dyhrman, S. T., Doney, S. C., and Webb, E. A.: Cross-basin comparison of phosphorus stress and nitrogen fixation in Trichodesmium, Limnol. Oceanogr., 54, 1438–1448, 10.4319/lo.2009.54.5.1438, 2009. · DOI
  31. Hynes, A. M., Webb, E. A., Doney, S. C., and Waterbury, J. B.: Comparison of cultured Trichodesmium (Cyanophyceae) with species characterized from the field, J. Phycol., 48, 196–210, 10.1111/j.1529-8817.2011.01096.x, 2012. · DOI
  32. Karl, D., Michaels, A., Bergman, B., Capone, D., Carpenter, E., Letelier, R., Lipschultz, F., Paerl, H., Sigman, D., and Stal, L.: Dinitrogen fixation in the world's oceans, Biogeochemistry, 57–58, 47–98, 10.1023/A:1015798105851, 2002. · DOI
  33. Kunde, K., Wyatt, N. J., González-Santana, D., Tagliabue, A., Mahaffey, C., and Lohan, M. C.: Iron Distribution in the Subtropical North Atlantic: The Pivotal Role of Colloidal Iron, Global Biogeochem. Cy., 33, 1532–1547, 10.1029/2019GB006326, 2019. · DOI
  34. Küpper, H., Šetlík, I., Seibert, S., Prášil, O., Šetlikova, E., Strittmatter, M., Levitan, O., Lohscheider, J., Adamska, I., and Berman-Frank, I.: Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation, New Phytol., 179, 784–798, 2008. · DOI
  35. Lee, M. D., Webb, E. A., Walworth, N. G., Fu, F. X., Held, N. A., Saito, M. A., and Hutchins, D. A.: Transcriptional activities of the microbial consortium living with the marine nitrogenfixing cyanobacterium Trichodesmium reveal potential roles in community-level nitrogen cycling, Appl. Environ. Microb., 84, e02026-17 10.1128/AEM.02026-17, 2018. · DOI
  36. Leventhal, G. E., Ackermann, M., and Schiessl, K. T.: Why microbes secrete molecules to modify their environment: The case of iron-chelating siderophores, J. R. Soc. Interface, 16, 20180674, 10.1098/rsif.2018.0674, 2019. · DOI
  37. López, C. V. G., García, M. d. C., Fernández, F. G. A., Bustos, C. S., Chisti, Y., and Sevilla, J. M. F.: Protein measurements of microalgal and cyanobacterial biomass, Bioresource Technol., 101, 7587–7591, 10.1016/j.biortech.2010.04.077, 2010. · DOI
  38. Lu, X. and Zhu, H.: Tube-Gel Digestion: A Novel Proteomic Approach for High Throughput Analysis of Membrane Proteins, Mol. Cell. Proteomics, 4, 1948–1958, 10.1074/mcp.M500138-MCP200, 2005. · DOI
  39. McGillicuddy, D. J.: Do Trichodesmium spp. populations in the North Atlantic export most of the nitrogen they fix?, Global Biogeochem. Cy., 28, 103–114, 10.1002/2013GB004652, 2014. · DOI
  40. Mills, M. M., Ridame, C., Davey, M., La Roche, J., and Geider, R. J.: Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic, Nature, 429, 292–294, 10.1038/nature02550, 2004 · DOI
  41. Mulholland, M. R. and Capone, D. G.: Nitrogen utilization and metabolism relative to patterns of N2 fixation in populations of Trichodesmium from the North Atlantic Ocean and Caribbean Sea, Mar. Ecol.-Prog. Ser., 188, 33–49, 1999. · DOI
  42. Ohki, K., Zehr, J. P., Falkowski, P. G., and Fujita, Y.: Regulation of nitrogen-fixation by different nitrogen sources in the marine non-heterocystous cyanobacterium Trichodesmium sp. NIBB1067, Arch. Microbiol., 156, 335–337, 10.1007/BF00248706, 1991. · DOI
  43. Orchard, E. D.: Phosphorus physiology of the marine Cyanobacterium Trichodesmium, Massachusetts Institute of Technology, 130, 81–122, 10.1575/1912/3366, 2010. · DOI
  44. Orchard, E. D., Webb, E. A., and Dyhrman, S. T.: Molecular analysis of the phosphorus starvation response in Trichodesmium spp., Environ. Microbiol., 11, 2400–2411, 10.1111/j.1462-2920.2009.01968.x, 2009. · DOI
  45. Orcutt, K. M., Gundersen, K., and Ammerman, J. W.: Intense ectoenzyme activities associated with Trichodesmium colonies in the Sargasso Sea, Mar. Ecol.-Prog. Ser., 478, 101–113, 10.3354/meps10153, 2013. · DOI
  46. Perez-Riverol, Y., Csordas, A., Bai, J., Bernal-Llinares, M., Hewapathirana, S., Kundu, D. J. Inuganti, A., Griss, J., Mayer G., Eisenacher, M., Perez, E., Uszkoriet, J., Pfeuffer, J., Sachsenberg, T., Yilmaz, S., Tiwary, S., Cox, J., Audain, E., Walzer, M., Januczak, A. F., Ternent, T., Brazma, A., and Vizcaíno, J. A.: The PRIDE database and related tools and resources in 2019: Improving support for quantification data, Nucleic Acids Res., 47, D442–D450, 10.1093/nar/gky1106, 2019. · DOI
  47. Polyviou, D., Hitchcock, A., Baylay, A. J., Moore, C. M., and Bibby, T. S.: Phosphite utilization by the globally important marine diazotroph Trichodesmium, Env. Microbiol. Rep., 7, 824–830, 10.1111/1758-2229.12308, 2015. · DOI
  48. Poorvin, L., Rinta-kanto, J. M., Hutchins, D. A., and Wilhelm, S. W.: Viral release of iron and its bioavailability to marine plankton, Limnol. Oceanogr., 49, 1734–1741, 2004. · DOI
  49. Reddy, R. J., Gajadhar, A. S., Swenson, E. J., Rothenberg, D. A., Curran, T. G., and White, F. M.: Early signaling dynamics of the epidermal growth factor receptor, P. Natl. Acad. Sci. USA, 113, 201521288, 10.1073/pnas.1521288113, 2016. · DOI
  50. Rouco, M., Frischkorn, K. R., Haley, S. T., and Alexander, H.: Transcriptional patterns identify resource controls on the diazotroph Trichodesmium in the Atlantic and Pacific oceans, ISME J., 1486–1495, 10.1038/s41396-018-0087-z, 2018. · DOI
  51. Rouwenhorst, R. J., Frank Jzn, J., Scheffers, W. A., and van Dijken, J. P.: Determination of protein concentration by total organic carbon analysis, J. Biochem. Bioph. Meth., 22, 119–128, 10.1016/0165-022X(91)90024-Q, 1991. · DOI
  52. Rubin, M., Berman-Frank, I., and Shaked, Y.: Dust-and mineral-iron utilization by the marine dinitrogen-fixer Trichodesmium, Nat. Geosci., 4, 529–534, 10.1038/ngeo1181, 2011. · DOI
  53. Saito, M. A., Goepfert, T. J., and Ritt, J. T.: Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability, Limnol. Oceanogr., 53, 276–290, 10.4319/lo.2008.53.1.0276, 2008. · DOI
  54. Saito, M. A., McIlvin, M. R., Moran, D. M., Goepfert, T. J., DiTullio, G. R., Post, A. F., and Lamborg, C. H.: Multiple nutrient stresses at intersecting Pacific Ocean biomes detected by protein biomarkers, Science, 345, 1173–1177, 10.1126/science.1256450, 2014. · DOI
  55. Saito, M. A., Dorsk, A., Post, A. F., McIlvin, M. R., Rappé, M. S., DiTullio, G. R., and Moran, D. M.: Needles in the blue sea: Sub-species specificity in targeted protein biomarker analyses within the vast oceanic microbial metaproteome, Proteomics, 15, 3521–3531, 10.1002/pmic.201400630, 2015. · DOI
  56. Sañudo-Wilhelmy, S. A., Kustka, A. B., Gobler, C. J., Hutchins, D. A., Yang, M., Lwiza, K., Burns, J., Capone, D. G., Raven, J. A., and Carpenter, E. J.: Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean, Nature, 411, 66–69, 10.1038/35075041, 2001. · DOI
  57. Sheridan, C. C.: The microbial and metazoan community associated with colonies of Trichodesmium spp.: a quantitative survey, J. Plankton Res., 24, 913–922, 10.1093/plankt/24.9.913, 2002. · DOI
  58. Shi, T., Sun, Y., and Falkowski, P. G.: Effects of iron limitation on the expression of metabolic genes in the marine cyanobacterium Trichodesmium erythraeum IMS101, Environ. Microbiol., 9, 2945–2956, 2007. · DOI
  59. Shih, P. M., Wu, D., Latifi, A., Axen, S. D., Fewer, D. P., Talla, E., Calteau, A., Cai, F., Tandeau de Marsac, N., Rippka, R., Herdman, M., Sivonen, K., Coursin, T., Laurent, T., Goodwin, L., Nolan, M., Davenport, K. W., Han, C. S., Rubin, E. M., Eisen, J. A., Woyke, T., Gugger, M., and Kerfeld, C. A.: Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing, P. Natl. Acad. Sci. USA, 110, 1053–1058, 10.1073/pnas.1217107110, 2013. · DOI · Paper page
  60. Snow, J. T., Polyviou, D., Skipp, P., Chrismas, N. A. M., Hitchcock, A., Geider, R., Moore, C. M., and Bibby, T. S.: Quantifying integrated proteomic responses to iron stress in the globally important marine diazotroph Trichodesmium, PLoS ONE, 10, 1–24, 10.1371/journal.pone.0142626, 2015. · DOI
  61. Sohm, J. A., Webb, E. A., and Capone, D. G.: Emerging patterns of marine nitrogen fixation, Nat. Rev. Microbiol., 9, 499–508, 10.1038/nrmicro2594, 2011. · DOI
  62. Strathmann, R. R.: Estimating Organic Carbon Content of Phytoplankton from Cell Volume or Plasma Volume, Limnol. Oceanogr., 12, 411–418, 1967. · DOI
  63. Sunda, W. G.: Feedback interactions between trace metal nutrients and phytoplankton in the ocean, Front. Microbiol., 3, 1–22, 10.3389/fmicb.2012.00204, 2012. · DOI
  64. Walworth, N. G., Fu, F.-X., Webb, E. A., Saito, M. A., Moran, D., Mcllvin, M. R., Lee, M. D., and Hutchins, D. A.: Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean, Nat. Commun., 7, 1–11, 10.1038/ncomms12081, 2016a. · DOI
  65. Walworth, N. G., Lee, M. D., Fu, F.-X., Hutchins, D. A., and Webb, E. A.: Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium, P. Natl. Acad. Sci. USA, 3, 201605202, 10.1073/pnas.1605202113, 2016b. · DOI
  66. Walworth, N. G., Fu, F. X., Lee, M. D., Cai, X., Saito, M. A., Webb, E. A., and Hutchins, D. A.: Nutrient-colimited Trichodesmium as a nitrogen source or sink in a future ocean, Appl. Environ. Microb., 84, 1–14, 10.1128/AEM.02137-17, 2018. · DOI
  67. Wang, Q., Li, H., and Post, A. F.: Nitrate assimilation genes of the marine diazotrophic, filamentous cyanobacterium Trichodesmium sp. strain WH9601, J. Bacteriol., 182, 1764–1767, 10.1128/JB.182.6.1764-1767.2000, 2000. · DOI
  68. Webb, E. A., Moffett, J. W., and Waterbury, J. B.: Iron Stress in Open-Ocean Cyanobacteria (Synechoccoccus, Trichodesmium, and Crocosphaera spp.): Identification of the IdiA Protein, Appl. Environ. Microb., 67, 5444–5452, 10.1128/AEM.67.12.5444-5452.2001, 2001. · DOI
  69. Webb, E. A., Jakuba, R. W., Moffett, J. W., and Dyhrman, S. T.: Molecular assessment of phosphorus and iron physiology in Trichodesmium populations from the western Central and western South Atlantic, Limnol. Oceanogr., 52, 2221–2232, 10.4319/lo.2007.52.5.2221, 2007. · DOI
  70. Wu, J. F., Sunda, W., Boyle, E. A., and Karl, D. M.: Phosphate depletion in the western North Atlantic Ocean, Science, 289, 759–762, 10.1126/Science.289.5480.759, 2000. · DOI
  71. Yamaguchi, T., Furuya, K., Sato, M., and Takahashi, K.: Phosphate release due to excess alkaline phosphatase activity in Trichodesmium erythraeum, Plankton Benthos Res., 11, 29–36, 10.3800/pbr.11.29, 2016. · DOI
  72. Yentsch, C. M., Yentsch, C. S., and Perras, J. P.: Alkaline phosphatase activity in the tropical marine blue-green alga Trichodesmium, Limnol. Oceanogr., 17, 72–774, 10.4319/lo.1972.17.5.0772, 1972. · DOI

Metadata

Authors
Held, N. A., Webb, E. A., McIlvin, M. M., Hutchins, D. A., Cohen, N. R., Moran, D. M., Kunde, K., Lohan, M. C., Mahaffey, C., Woodward, E. M. S., & Saito, M. A.
Affiliations
  • Massachusetts Institute of Technology (US)
  • University of Southern California (US)
  • Woods Hole Oceanographic Institution (US)
  • National Oceanography Centre (GB)
  • University of Liverpool (GB)
  • Plymouth Marine Laboratory (GB)
Corresponding author
  • Held, Noelle A.
  • Webb, Eric A.
  • Hutchins, David A.
  • Cohen, Natalie R.
  • Moran, Dawn M.
  • Kunde, Korinna
  • Lohan, Maeve C.
  • Mahaffey, Claire
  • Woodward, E. Malcolm S.
  • Saito, Mak A.
ORCID
Venue
Biogeosciences
Publisher
Copernicus GmbH
Published
2020-05-12
Volume
17
Issue
9
Pages
2537-2551
ISSN
  • 1726-4170 (ISSN-L)
  • 1726-4189
DOI
10.5194/bg-17-2537-2020
OpenAlex
W2998863824
Cited by
45
References
1
Citations by year
2026: 2 · 2025: 5 · 2024: 11 · 2023: 8 · 2022: 7 · 2021: 7 · 2020: 5
FWCI
3.36
Type
journal article
Language
en
Open access
Licence
Locations
  • Biogeosciences (publishedVersion, cc-by)
  • Marine Biological Association (acceptedVersion)
  • ePrints Soton (University of Southampton) (submittedVersion)
  • DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by)
  • Open Access Server of the Woods Hole Scientific Community (Woods Hole Scientific Community) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Division of Graduate Education (1122274)
  • Division of Ocean Sciences (1657755, 1657757, 1851222)
  • Directorate for Geosciences (1639714)
  • Gordon and Betty Moore Foundation (3782)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine Plankton and Biogeochemistry
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Metalloenzymes and iron-sulfur proteins
  • Physical Sciences › Environmental Science › Environmental Chemistry › Aquatic Ecosystems and Phytoplankton Dynamics
Keywords
Trichodesmium, iron stress, phosphate stress, nitrogen fixation, nitrogenase, organic nitrogen uptake, nutrient acquisition, colony formation, marine diazotrophs, North Atlantic, metaproteomics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review