Basin-wide N2 fixation in the deep waters of the Mediterranean Sea

Global Biogeochemical Cycles

Volumn 30, Issue 6, 2016, Pages 952-961

  Benavides, Mar ^a,b   Bonnet, Sophie ^a   Hernández, Nauzet ^b   Martínez Pérez, Alba María ^c   Nieto Cid, Mar ^c   Álvarez Salgado, Xosé Antón ^c   Baños, Isabel ^b   Montero, María F ^b   Mazuecos, Ignacio P ^d   Gasol, Josep M ^e   Osterholz, Helena ^f   Dittmar, Thorsten ^f   Berman Frank, Ilana ^g   Arístegui, Javier ^b  

^a STATION MARINE D ENDOUME   (France)

^b UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^c INSTITUTO DE INVESTIGACIONES MARINAS   (Spain)

^d UNIVERSITY OF GRANADA   (Spain)

^e INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^f UNIVERSITY OF OLDENBURG   (Germany)

^g BAR ILAN UNIVERSITY   (Israel)

Author keywords

diazotrophy

Indexed keywords

CHLOROPHYLL; DEEP WATER; EUPHOTIC ZONE; NITRIFYING BACTERIUM; NITROGEN FIXATION; NUTRITION; ORGANIC MATTER; PEPTIDE; WATER COLUMN; WATER MASS;

MEDITERRANEAN SEA;

EID: 84978438784     PISSN: 08866236     EISSN: 19449224     Source Type: Journal    
DOI: 10.1002/2015GB005326     Document Type: Article

References (63)

1. Arístegui, J., and M. F. Montero (1995), The relationship between community respiration and ETS activity in the ocean, J. Plankton Res., 17(7), 1563–1571.
2. Arístegui, J., J. M. Gasol, C. M. Duarte, and G. J. Herndl (2009), Microbial oceanography of the dark ocean's pelagic realm, Limnol. Oceanogr., 54(5), 1501–1529, doi:10.4319/lo.2009.54.5.1501.
3. Bar-Zeev, E., T. Yogev, D. Man-Aharonovich, N. Kress, B. Herut, O. Béjà, and I. Berman-Frank (2008), Seasonal dynamics of the endosymbiotic, nitrogen-fixing cyanobacterium Richelia intracellularis in the eastern Mediterranean Sea, ISME J., 2(9), 911–923, doi:10.1038/ismej.2008.56.
4. 2 fixation related to organic matter composition in the Solomon and Bismarck Seas (Southwest Pacific), PLOS ONE, 10(12), e0143775, doi:10.1371/journal.pone.0143775.
5. Bentzon-Tilia, M., I. Severin, L. H. Hansen, and L. Riemann (2015), Genomics and ecophysiology of heterotrophic nitrogen-fixing bacteria isolated from estuarine surface water, mBio, 6(4), e00929-15, doi:10.1128/mBio.00929-15.
6. Berman-Frank, I., P. Lundgren, and P. Falkowski (2003), Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria, Res. Microbiol., 154(3), 157–164, doi:10.1016/S0923-2508(03)00029-9.
7. Bethoux, J. P., and G. Copin-Montegut (1986), Biological fixation of atmospheric nitrogen in the Mediterranean Sea, Limnol. Oceanogr., 31(6), 1353–1358, doi:10.4319/lo.1986.31.6.1353.
8. Bonnet, S., O. Grosso, and T. Moutin (2011), Planktonic dinitrogen fixation along a longitudinal gradient across the Mediterranean Sea during the stratified period (BOUM cruise), Biogeosciences, 8(8), 2257–2267, doi:10.5194/bg-8-2257-2011.
9. 2 fixation in the eastern tropical South Pacific Ocean, PLOS ONE, 8(12), e81265, doi:10.1371/journal.pone.0081265.s001.
10. Boutrif, M., M. Garel, M. T. Cottrell, and C. Tamburini (2011), Assimilation of marine extracellular polymeric substances by deep-sea prokaryotes in the NW Mediterranean Sea, Environ. Microbiol. Rep., 3(6), 705–709, doi:10.1111/j.1758-2229.2011.00285.x.
11. Capone, D. G., and A. N. Knapp (2007), Oceanography: A marine nitrogen cycle fix?, Nature, 445(7124), 159–160, doi:10.1038/445159a.
12. Coble, P. G. (1996), Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy, Mar. Chem., 51(6), 325–346, doi:10.1016/0304-4203(95)00062-3.
13. 15N-labeled nitrate and ammonium and consequences for nitrogen fixation measurements, PLOS ONE, 9(10), e110335, doi:10.1371/journal.pone.0110335.
14. Dekaezemacker, J., S. Bonnet, O. Grosso, T. Moutin, M. Bressac, and D. G. Capone (2013), Evidence of active dinitrogen fixation in surface waters of the eastern tropical South Pacific during El Niño and La Niña events and evaluation of its potential nutrient controls, Global Biogeochem. Cycles, 27, 768–779, doi:10.1002/gbc.20063.
15. Deutsch, C., J. L. Sarmiento, D. M. Sigman, N. Gruber, and J. P. Dunne (2007), Spatial coupling of nitrogen inputs and losses in the ocean, Nature, 445(7124), 163–167, doi:10.1038/nature05392.
16. Dittmar, T., B. Koch, N. Hertkorn, and G. Kattner (2008), A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater, Limnol. Oceanogr. Methods, 6, 230–235, doi:10.4319/lom.2008.6.230.
17. Farnelid, H., A. F. Andersson, S. Bertilsson, W. A. Al-Soud, L. H. Hansen, S. Sørensen, G. F. Steward, Å. Hagström, and L. Riemann (2011), Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria, PLOS ONE, 6(4), e19223, doi:10.1371/journal.pone.0019223.t001.
18. Farnelid, H., M. Bentzon-Tilia, A. F. Andersson, S. Bertilsson, G. Jost, M. Labrenz, K. Jürgens, and L. Riemann (2013), Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea, ISME J., 7(7), 1413–1423, doi:10.1038/ismej.2013.26.
19. Fernández, C., L. Farías, and O. Ulloa (2011), Nitrogen fixation in denitrified marine waters, PLOS ONE, 6(6), e20539, doi:10.1371/journal.pone.0020539.t001.
20. Gasol, J. M., and P. del Giorgio (2000), Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities, Sci. Mar., 64(2), 197–224.
21. Grasshoff, K., M. Ehrhardt, K. Kremling, and M. Ehrhardt (Eds.) (1999), Methods of Seawater Analysis, 3rd ed., Verlag Chemie, Weinheim, Germany.
22. Green, S. A., and N. V. Blough (1994), Optical absorption and fluorescence properties of chromophoric dissolved organic matter in natural waters, Limnol. Oceanogr., 39(8), 1903–1916, doi:10.4319/lo.1994.39.8.1903.
23. Großkopf, T., W. Mohr, T. Baustian, H. Schunck, D. Gill, M. M. M. Kuypers, G. Lavik, R. A. Schmitz, D. W. R. Wallace, and J. LaRoche (2012), Doubling of marine dinitrogen-fixation rates based on direct measurements, Nature, 488(7411), 361–364, doi:10.1038/nature11338.
24. Hamersley, M. R., K. A. Turk, A. Leinweber, N. Gruber, J. P. Zehr, T. Gunderson, and D. G. Capone (2011), Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight, Aquat. Microb. Ecol., 63(2), 193–205, doi:10.3354/ame01494.
25. Hewson, I., P. H. Moisander, K. M. Achilles, C. A. Carlson, B. D. Jenkins, E. A. Mondragon, A. E. Morrison, and J. P. Zehr (2007), Characteristics of diazotrophs in surface to abyssopelagic waters of the Sargasso Sea, Aquat. Microb. Ecol., 46, 15–30, doi:10.3354/ame046015.
26. Huertas, I. E., A. F. Ríos, J. García-Lafuente, G. Navarro, A. Makaoui, A. Sánchez-Román, S. Rodriguez-Galvez, A. Orbi, J. Ruíz, and F. F. Pérez (2012), Atlantic forcing of the Mediterranean oligotrophy, Global Biogeochem. Cycles, 26, GB2022, doi:10.1029/2011GB004167.
27. 2 fixation in the open Mediterranean Sea, Geophys. Res. Lett., 37, L03608, doi:10.1029/2009GL041635.
28. Kirchman, D., E. K'nees, and R. Hodson (1985), Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems, Appl. Environ. Microbiol., 49(3), 599–607.
29. 2-enriched water for nitrogen fixation assessments: Evaluation, application and recommendations, Front. Microbiol., doi:10.3389/fmicb.2015.00769.
30. Koch, B. P., and T. Dittmar (2006), From mass to structure: An aromaticity index for high-resolution mass data of natural organic matter, Rapid Commun. Mass Spectrom., 20(5), 926–932, doi:10.1002/rcm.2386.
31. Krom, M. D., and B. Herut (2004), Nutrient budget for the Eastern Mediterranean: Implications for phosphorus limitation, Limnol. Oceanogr., 49(5), 1582–1592, doi:10.4319/lo.2004.49.5.1582.
32. Le Moal, M., H. Collin, and I. C. Biegala (2011), Intriguing diversity among diazotrophic picoplankton along a Mediterranean transect: A dominance of rhizobia, Biogeosciences, 8(3), 827–840, doi:10.5194/bg-8-827-2011.
33. Loescher, C. R., et al. (2014), Facets of diazotrophy in the oxygen minimum zone waters off Peru, ISME J., 8, 2180–2192, doi:10.1038/ismej.2014.71.
34. Ludwig, W., E. Dumont, M. Meybeck, and S. Heussner (2009), River discharges of water and nutrients to the Mediterranean and Black Sea: Major drivers for ecosystem changes during past and future decades? Prog. Oceanogr., 80(3–4), 199–217, doi:10.1016/j.pocean.2009.02.001.
35. Luna, G. M., S. Bianchelli, F. Decembrini, E. De Domenico, R. Danovaro, and A. Dell'Anno (2012), The dark portion of the Mediterranean Sea is a bioreactor of organic matter cycling, Global Biogeochem. Cycles, 26, GB2017, doi:10.1029/2011GB004168.
36. Macías, D., A. Stips, and E. Garcia-Gorriz (2014), The relevance of deep chlorophyll maximum in the open Mediterranean Sea evaluated through 3D hydrodynamic-biogeochemical coupled simulations, Ecol. Modell., 281, 26–37, doi:10.1016/j.ecolmodel.2014.03.002.
37. Man-Aharonovich, D., N. Kress, E. B. Zeev, I. Berman-Frank, and O. Béjà (2007), Molecular ecology of nifH genes and transcripts in the eastern Mediterranean Sea, Environ. Microbiol., 9(9), 2354–2363, doi:10.1111/j.1462-2920.2007.01353.x.
38. Manca, B., M. Burca, A. Giorgetti, C. Coatanoan, M. J. Garcia, and A. Iona (2004), Physical and biochemical averaged vertical profiles in the Mediterranean regions: An important tool to trace the climatology of water masses and to validate incoming data from operational oceanography, J. Mar. Syst., 48(1–4), 83–116, doi:10.1016/j.jmarsys.2003.11.025.
39. Markaki, Z., M. D. Loÿe-Pilot, K. Violaki, L. Benyahya, and N. Mihalopoulos (2010), Variability of atmospheric deposition of dissolved nitrogen and phosphorus in the Mediterranean and possible link to the anomalous seawater N/P ratio, Mar. Chem., 120(1–4), 187–194, doi:10.1016/j.marchem.2008.10.005.
40. Meador, T. B., A. Gogou, G. Spyres, G. J. Herndl, E. Krasakopoulou, S. Psarra, T. Yokokawa, D. De Corte, V. Zervakis, and D. J. Repeta (2010), Biogeochemical relationships between ultrafiltered dissolved organic matter and picoplankton activity in the Eastern Mediterranean Sea, Deep-Sea Res., Part II, 57(16), 1460–1477, doi:10.1016/j.dsr2.2010.02.015.
41. 2 fixation, Appl. Environ. Microbiol., 62(3), 986–993.
42. Mulholland, M. R., P. W. Bernhardt, J. L. Blanco-Garcia, A. Mannino, K. Hyde, E. Mondragon, K. Turk, P. H. Moisander, and J. P. Zehr (2012), Rates of dinitrogen fixation and the abundance of diazotrophs in North American coastal waters between Cape Hatteras and Georges Bank, Limnol. Oceanogr., 57(4), 1067–1083, doi:10.4319/lo.2012.57.4.1067.
43. 2 fixation in nitrogen-depleted aerobic marine waters, Appl. Environ. Microbiol., 53(5), 1078–1087.
44. Pantoja, S., D. J. Repeta, J. P. Sachs, and D. M. Sigman (2002), Stable isotope constraints on the nitrogen cycle of the Mediterranean Sea water column, Deep-Sea Res., Part I, 49(9), 1609–1621, doi:10.1016/S0967-0637(02)00066-3.
45. Passow, U., and A. L. Alldredge (1995), A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP), Limnol. Oceanogr., 40(7), 1326–1335, doi:10.4319/lo.1995.40.7.1326.
46. Pujo-Pay, M., P. Conan, L. Oriol, V. Cornet-Barthaux, C. Falco, J. F. Ghiglione, C. Goyet, T. Moutin, and L. Prieur (2011), Integrated survey of elemental stoichiometry (C, N, P) from the western to eastern Mediterranean Sea, Biogeosciences, 8(4), 883–899, doi:10.5194/bg-8-883-2011.
47. Rahav, E., B. Herut, A. Levi, M. R. Mulholland, and I. Berman-Frank (2013a), Springtime contribution of dinitrogen fixation to primary production across the Mediterranean Sea, Ocean Sci., 9(3), 489–498, doi:10.5194/os-9-489-2013.
48. Rahav, E., B. Herut, M. R. Mulholland, B. Voß, D. Stazic, C. Steglich, W. R. Hess, and I. Berman-Frank (2013b), Contribution of dinitrogen fixation to bacterial and primary productivity in the Gulf of Aqaba (Red Sea), Biogeosci. Discuss., 10(6), 10,327–10,361, doi:10.5194/bgd-10-10327-2013.
49. Rahav, E., E. Bar-Zeev, S. Ohayon, H. Elifantz, N. Belkin, B. Herut, M. R. Mulholland, and I. Berman-Frank (2013c), Dinitrogen fixation in aphotic oxygenated marine environments, Front. Microbiol., 4(227), 1–11, doi:10.3389/fmicb.2013.00227/abstract.
50. Rahav, E., B. Herut, M. R. Mulholland, N. Belkin, H. Elifantz, and I. Berman-Frank (2015), Heterotrophic and autotrophic contribution to dinitrogen fixation in the Gulf of Aqaba, Mar. Ecol. Prog. Ser., 522, 67–77, doi:10.3354/meps11143.
51. Riemann, L., H. Farnelid, and G. F. Steward (2010), Nitrogenase genes in non-cyanobacterial plankton: Prevalence, diversity and regulation in marine waters, Aquat. Microb. Ecol., 61(3), 235–247, doi:10.3354/ame01431.
52. Rodellas, V., J. Garcia-Orellana, P. Masqué, M. Feldman, and Y. Weinstein (2015), Submarine groundwater discharge as a major source of nutrients to the Mediterranean Sea, Proc. Natl. Acad. Sci. U.S.A., 112(13), 3926–3930, doi:10.1073/pnas.1419049112.
53. Sachs, J. P. (1999), Oligotrophy and nitrogen fixation during eastern Mediterranean sapropel events, Science, 286(5449), 2485–2488, doi:10.1126/science.286.5449.2485.
54. Santinelli, C., B. B. Manca, G. P. Gasparini, L. Nannicini, and A. Seritti (2006), Vertical distribution of dissolved organic carbon (DOC) in the Mediterranean Sea, Clim. Res., 31, 205–216, doi:10.3354/cr031205.
55. Santinelli, C., L. Nannicini, and A. Seritti (2010), DOC dynamics in the meso and bathypelagic layers of the Mediterranean Sea, Deep-Sea Res., Part II, 57(16), 1446–1459, doi:10.1016/j.dsr2.2010.02.014.
56. Seidel, M., M. Beck, T. Riedel, and H. Waska (2014), Biogeochemistry of dissolved organic matter in an anoxic intertidal creek bank, Geochim. Cosmochim. Acta, 140, 418–434, doi:10.1016/j.gca.2014.05.038.
57. Severin, I., M. Bentzon-Tilia, P. H. Moisander, and L. Riemann (2015), Nitrogenase expression in estuarine bacterioplankton influenced by organic carbon and availability of oxygen, FEMS Microbiol. Lett., doi:10.1093/femsle/fnv105.
58. 3H-leucine, Mar. Microb. Food Webs, 6(2), 107–114.
59. United Nations Educational, Scientific and Cultural Organization (1986), Progress on oceanographic tables and standards 1983–1986: Work and recommendations of the UNESCO/SCOR/ICES/IAPSO Joint Panel.
60. Weishaar, J. L., G. R. Aiken, B. A. Bergamaschi, M. S. Fram, R. Fujii, and K. Mopper (2003), Evaluation of specific ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon, Environ. Sci. Technol., 37(20), 4702–4708, doi:10.1021/es030360x.
61. Yogev, T., E. Rahav, E. Bar-Zeev, D. Man-Aharonovich, N. Stambler, N. Kress, O. Béjà, M. R. Mulholland, B. Herut, and I. Berman-Frank (2011), Is dinitrogen fixation significant in the Levantine Basin, East Mediterranean Sea?, Environ. Microbiol., 13(4), 854–871, doi:10.1111/j.1462-2920.2010.02402.x.
62. Zehr, J. P. (2011), Nitrogen fixation by marine cyanobacteria, Trends Microbiol., 19(4), 162–173, doi:10.1016/j.tim.2010.12.004.
63. Zehr, J. P., B. D. Jenkins, S. M. Short, and G. F. Steward (2003), Nitrogenase gene diversity and microbial community structure: A cross-system comparison, Environ. Microbiol., 5(7), 539–554, doi:10.1046/j.1462-2920.2003.00451.x.