Contribution of mono and polysaccharides to heterotrophic N 2 fixation at the eastern Mediterranean coastline

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Rahav, E ^a   Giannetto, M J ^b   Bar Zeev, E ^c  

^a ISRAEL OCEANOGRAPHIC AND LIMNOLOGICAL RESEARCH   (Israel)

^b Yale University   (United States)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; NITROGENASE REDUCTASE; OXIDOREDUCTASE;

MEDITERRANEAN SEA; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PHYSIOLOGY; PROTEOBACTERIA;

BACTERIAL PROTEINS; MEDITERRANEAN SEA; NITROGEN FIXATION; OXIDOREDUCTASES; POLYSACCHARIDES, BACTERIAL; PROTEOBACTERIA; WATER MICROBIOLOGY;

EID: 84975034906     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27858     Document Type: Article

References (60)

1. Großkopf, T. & Laroche, J. Direct and indirect costs of dinitrogen fixation in Crocosphaera watsonii WH8501 and possible implications for the nitrogen cycle. Frontiers in microbiology 3, 236 (2012).
2. Capone, D. G., Zehr, J. P., Paerl, H. W., Bergman, B. & Carpenter, E. J. Trichodesmium, a globally significant marine cyanobacterium. Science 276, 1221-1229 (1997).
3. Zehr, J. P. Nitrogen fixation by marine cyanobacteria. Trends in microbiology 19, 162-173 (2011).
4. Halm, H. et al. Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. The ISME journal 6, 1238-1249 (2012).
5. Farnelid, H., Bentzon-tilia, M., Andersson, A. F. & Bertilsson, S. Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. The ISME journal 7, 1413-1423 (2013).
6. Riemann, L., Farnelid, H. & Steward, G. Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquatic Microbial Ecology 61, 235-247 (2010).
7. Bentzon-Tilia, M. et al. Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. The ISME journal 1-13 (2014).
8. Rahav, E. et al. Dinitrogen fixation in aphotic oxygenated marine environments. Frontiers in Microbiology 4, 227 (2013).
9. Dyhrman, S. T. & Haley, S. T. Phosphorus scavenging in the unicellular marine diazotroph Crocosphaera watsonii. Applied and Environmental Microbiology 72, 1452-1458 (2006).
10. Berman-Frank, I., Cullen, J. T., Shaked, Y., Sherrell, R. M. & Falkowski, P. G. Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnology and Oceanography 46, 1249-1260 (2001).
11. Mills, M. M., Ridame, C., Davey, M., La Roche, J. & Geider, R. J. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429, 292-294 (2004).
12. Moisander, P. H. et al. Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean. The ISME journal 6, 733-744 (2012).
13. Benavides, M. et al. Mesopelagic N2 fixation related to organic matter composition in the Solomon and Bismarck Seas (Southwest Pacific). Plos One 10, e0143775 (2015).
14. Dekaezemacker, J. et al. Evidence of active dinitrogen fixation in surface waters of the eastern tropical South Pacific during El Nino and la Nina events and evaluation of its potential nutrient controls. Global Biogeochemical Cycles 27, 768-779 (2013).
15. Bonnet, S. et al. Aphotic N2 fixation in the eastern tropical south Pacific Ocean. PloS one 8, e81265 (2013).
16. Loescher, C. R. et al. Facets of diazotrophy in the oxygen minimum zone waters off Peru. The ISME journal 8,1-13 (2014).
17. Bar-Zeev, E. et al. Transparent exopolymer particle (TEP) dynamics in the eastern Mediterranean Sea. Marine Ecology Progress Series 431, 107-118 (2011).
18. Raveh, O., David, N., Rilov, G. & Rahav, E. The temporal dynamics of coastal phytoplankton and bacterioplankton in the Eastern Mediterranean Sea. Plos One 10, e0140690 (2015).
19. Sachs, J. P. & Repeta, D. J. Oligotrophy and nitrogen fixation during Eastern Mediterranean sapropel events. Science 286, 2485-2488 (1999).
20. Bethoux, J. P., Morin, P. Madec C. & Gentili, B. Phosphorus and nitrogen behavoir in the Mediterranean Sea. Deep-Sea Research 39, 1641-1654 (1992).
21. Man-Aharonovich, D., Kress, N., Zeev, E. B., Berman-Frank, I. & Béja, O. Molecular ecology of nifH genes and transcripts in the eastern Mediterranean Sea. Environmental microbiology 9, 2354-2363 (2007).
22. Bar-Zeev, E. et al. Seasonal dynamics of the endosymbiotic, nitrogen-fixing cyanobacterium Richelia intracellularis in the eastern Mediterranean Sea. The ISME journal 2, 911-923 (2008).
23. Yogev, T. et al. Is dinitrogen fixation significant in the Levantine Basin, East Mediterranean Sea? Environmental microbiology 13, 854-871 (2011).
24. Ibello, V., Cantoni, C., Cozzi, S. & Civitarese, G. First basin-wide experimental results on N2 fixation in the open Mediterranean Sea. Geophysical Research Letters 37, 1-5 (2010).
25. Bonnet, S., Grosso, O. & Moutin, T. Planktonic dinitrogen fixation along a longitudinal gradient across the Mediterranean Sea during the stratified period (BOUM cruise). Biogeosciences 8, 2257-2267 (2011).
26. Rahav, E. et al. Uncoupling between dinitrogen fixation and primary productivity in the eastern Mediterranean Sea. Journal of Geophysical Research: Biogeosciences 118, 195-202 (2013).
27. Spatharis, S., Skliris, N. & Meziti, A. First record of a Trichodesmium erythraeum bloom in the Mediterranean Sea. Canadian Journal of Fisheries and Aquatic Sciences 69, 1444-1455 (2012).
28. Ridame, C., Guieu, C. & L'Helguen, S. Strong stimulation of N2 fixation in oligotrophic Mediterranean Sea: Results from dust addition in large in situ mesocosms. Biogeosciences 10, 7333-7346 (2013).
29. Rahav, E. et al. Heterotrophic and autotrophic contribution to dinitrogen fixation in the Gulf of Aqaba. Marine Ecology Progress Series 522, 67-77 (2015).
30. Kress, N. & Herut, B. Spatial and seasonal evolution of dissolved oxygen and nutrients in the Southern Levantine Basin (Eastern Mediterranean Sea): chemical characterization of the water masses and inferences on the N:P ratios. Deep Sea Research Part I: Oceanographic Research Papers 48, 2347-2372 (2001).
31. Welschmeyer, N. A. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39, 1985-1992 (1994).
32. Steemann-Nielsen, E. On the determination of the activity for measuring primary production. J Cons Int Explor Mer 18, 117-140 (1952).
33. Simon, M., Alldredge, A. & Azam, F. Bacterial carbon dynamics on marine snow. Marine Ecology Progress Series 65, 205-211 (1990).
34. Simon, M., Alldredge, A. & Azam, F. Protein-content and protein-synthesis rates of planktonic marine-bacteria. Marine Ecology Progress Series 51, 201-213 (1989).
35. Vaulot, D. & Marie, D. Diel variability of photosynthetic picoplankton in the equatorial Pacific. Applied and environmental microbiology 104, 3297-3310 (1999).
36. Carpenter, J. H. The Chesapeake bay institute technique for the Winkler dissolved oxygen method. Limnology and Oceanography 10, 141-143 (1965).
37. Del Giorgio, P. a. & Cole, J. J. Bacterial growth efficiency in natural aquatic systems. Annual Review of Ecology and Systematics 29, 503-541 (1998).
38. Bar-zeev, E. & Rahav, E. Microbial metabolism of transparent exopolymer particles during the summer months along a eutrophic estuary system. Frontiers in microbiology 6, 1-13 (2015).
39. Passow, U. & Alldredge, A. L. A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limonology And Oceanography 40, 1326-1335 (1995).
40. Engel, a. & Passow, U. Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their Alcian Blue adsorption. Marine Ecology Progress Series 219, 1-10 (2001).
41. Hoppe, H.-G. Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates Marine Ecology Progress Series 11, 299-308 (1983).
42. Mohr, W., Großkopf, T., Wallace, D. W. R. & Laroche, J. Methodological underestimation of oceanic nitrogen fixation rates. PLos One 49, (2010).
43. Zehr, J. P. & McReynolds, L. A. Use of degenerate oligonucleotides for amplification of the nifH gene from the marine cyanobacterium Trichodesmium thiebautii. Applied and Environmental Microbiology 55, 2522-2526 (1989).
44. Caporaso, J. G., Kuczynski, J. & Stombaugh, J. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7, 335-336 (2010).
45. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
46. Heller, P., Tripp, H. J., Turk-Kubo, K. & Zehr, J. P. ARBitrator: A software pipeline for on-demand retrieval of auto-curated nifH sequences from GenBank. Bioinformatics 30, 1-8 (2014).
47. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Molecular Biology and Evolution 26, 1641-1650 (2009).
48. Pulido-Villena, E., Ghiglione, J. F., Ortega-Retuerta, E., Van-Wambeke, F. & Zohary, T. In Life in the Mediterranean Sea: A Look at Habitat Changes 227-265 (Nova Science Publishers, 2012).
49. Chien, Y. T. & Zinder, S. H. Cloning, functional organization, transcript studies, and phylogenetic analysis of the complete nitrogenase structural genes (nifHDK2) and associated genes in the archaeon Methanosarcina barkeri 227. Journal of Bacteriology 178, 143-148 (1996).
50. Rahav, E., Herut, B., Levi, Adi, Mulholland, M. R. & Berman-Frank, I. Springtime contribution of dinitrogen fixation to primary production across the Mediterranean Sea. Ocean Science 9, 489-498 (2013).
51. Rahav, E., Ovadia, G., Paytan, A. & Herut, B. Contribution of airborne microbes to bacterial production and N2 fixation in seawater upon aerosol deposition. Geophys. Research Letters. 43, 1-9 (2016).
52. Zohary, T. et al. P-limited bacteria but N and P co-limited phytoplankton in the Eastern Mediterranean-a microcosm experiment. Deep Sea Research Part II: Topical Studies in Oceanography 52, 3011-3023 (2005).
53. Steppe, T. F., Pinckney, J. L., Dyble, J. & Paerl, H. W. Diazotrophy in Modern Marine Bahamian Stromatolites. Microbial ecology 41, 36-44 (2001).
54. Bar-Zeev, E., Passow, U., Romero-Vargas Castrillón, S. & Elimelech, M. Transparent exopolymer particles: from aquatic environments and engineered systems to membrane biofouling. Environmental Science & Technology 49, 691-707 (2015).
55. Radi, T., Ivanci, I., Fuks, D. & Radi, J. Marine bacterioplankton production of polysaccharidic and proteinaceous particles under different nutrient regimes. FEMS microbiology ecology 58, 333-342 (2006).
56. Ducklow, H. W. et al. Constraining bacterial production, conversion efficiency and respiration in the Ross Sea, Antarctica, January-February, 1997. Deep Sea Research Part II: Topical Studies in Oceanography 47, 3227-3247 (2000).
57. Bar-Zeev, E., Berman-Frank, I., Girshevitz, O. & Berman, T. Revised paradigm of aquatic biofilm formation facilitated by microgel transparent exopolymer particles. Proceedings of the National Academy of Sciences 109, 9119-9124 (2012).
58. Azam, F. & Malfatti, F. Microbial structuring of marine ecosystems. Nature reviews Microbiology 5, 782-791 (2007).
59. Klawonn, I., Bonaglia, S., Bruchert, V. & Ploug, H. Aerobic and anaerobic nitrogen transformation processes in N2-fixing cyanobacterial aggregates. The ISME Jornal 9, 1456-1466 (2015).
60. Bentzon-Tilia, M., Severin, I., Hansen, L. H. & Riemann, L. Bacteria Isolated from Estuarine Surface Water. American Society for Microbiology 6, 1-11 (2015).