Facets of diazotrophy in the oxygen minimum zone waters off Peru

ISME Journal

Volumn 8, Issue 11, 2014, Pages 2180-2192

  Loescher, Carolin R ^a   Großkopf, Tobias ^b,c   Desai, Falguni D ^b,d   Gill, Diana ^b   Schunck, Harald ^a,b   Croot, Peter L ^e   Schlosser, Christian ^f   Neulinger, Sven C ^a   Pinnow, Nicole ^a   Lavik, Gaute ^g   Kuypers, Marcel M M ^g   Laroche, Julie ^b,d   Schmitz, Ruth A ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^c UNIVERSITY OF WARWICK   (United Kingdom)

^d DALHOUSIE UNIVERSITY   (Canada)

^e NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^f UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^g MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

Author keywords

heterotrophic N2 fixation; nifH diversity; oxygen minimum zone off Peru

Indexed keywords

CLADISTICS; CYANOBACTERIUM; GENETIC MARKER; NICHE; NITROGEN FIXATION; OXYGEN MINIMUM LAYER; WATER COLUMN;

PERU;

NITRIC ACID DERIVATIVE; NITROGENASE REDUCTASE; OXIDOREDUCTASE; OXYGEN; SEA WATER;

ARCHAEON; BACTERIUM; CHEMISTRY; CLASSIFICATION; CYANOBACTERIUM; DENITRIFICATION; GENETICS; HETEROTROPHY; ISOLATION AND PURIFICATION; MICROBIOLOGY; NITROGEN FIXATION; PERU; PHYLOGENY; PROTEOBACTERIA; SEA;

ARCHAEA; BACTERIA; CYANOBACTERIA; DENITRIFICATION; HETEROTROPHIC PROCESSES; NITRATES; NITROGEN FIXATION; OCEANS AND SEAS; OXIDOREDUCTASES; OXYGEN; PERU; PHYLOGENY; PROTEOBACTERIA; SEAWATER;

EID: 84908234152     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.71     Document Type: Article

References (50)

1. Bopp L, Le Quere C, Heimann M, Manning AC, Monfray P. (2002). Climate-induced oceanic oxygen fluxes: implications for the contemporary carbon budget. Global Biogeochem Cycles 16: 14.
2. Bruland KW, Franks RP, Knauer GA, Martin JH. (1979). Sampling and analytical methods for the determination of copper, cadmium, zinc, and nickel at the nanogram per liter level in sea water. Anal Chim Acta 105: 233-245.
3. Bruland KW, Rue EL, Smith GJ, DiTullio GR. (2005). Iron, macronutrients and diatom blooms in the Peru upwelling regime: brown and blue waters of Peru. Mar Chem 93: 81-103.
4. Capone D. (2008). The marine nitrogen cycle. Microbe 3: 186-192.
5. Capone DG, Burns JA, Montoya JP, Subramaniam A, Mahaffey C, Gunderson T et al. (2005). Nitrogen fixation by Trichodesmium spp.: an important source of new nitrogen to the tropical and subtropical North Atlantic Ocean. Global Biogeochem Cycles 19: 17.
6. Church MJ, Jenkins BD, Karl DM, Zehr JP. (2005). Vertical distributions of nitrogen-fixing phylotypes at Stn ALOHA in the oligotrophic North Pacific Ocean. Aquat Microb Ecol 38: 3-14.
7. Codispoti LA. (2007). An oceanic fixed nitrogen sink exceeding 400 Tg Na(-1) vs the concept of homeostasis in the fixed-nitrogen inventory. Biogeosciences 4: 233-253.
8. Codispoti LA. (2010). Interesting times for marine N2O. Science 327: 1339-1340.
9. Danielsson L-G, Magnusson B, Westerlund S. (1978). An improved metal extraction procedure for the determination of trace metals in sea water by atomic absorption spectrometry with electrothermal atomization. Anal Chim Acta 98: 47-57.
10. Deutsch C, Gruber N, Key RM, Sarmiento JL, Ganachaud A. (2001). Denitrification and N2 fixation in the Pacific Ocean. Global Biogeochem Cycles 15: 483-506.
11. Deutsch C, Sarmiento JL, Sigman DM, Gruber N, Dunne JP. (2007). Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445: 163-167.
12. Duce RA, LaRoche J, Altieri K, Arrigo KR, Baker AR, Capone DG et al. (2008). Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320: 893-897.
13. Falcon LI, Cipriano F, Chistoserdov AY, Carpenter EJ. (2002). Diversity of diazotrophic unicellular cyanobacteria in the tropical North Atlantic Ocean. Appl Environ Microbiol 68: 5760-5764.
14. Farnelid H, Bentzon-Tilia M, Andersson AF, Bertilsson S, Jost G, Labrenz M et al. (2013). Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. ISME J 7: 1413-1423.
15. Farnelid H, Andersson AF, Bertilsson S, Al-Soud WA, Hansen LH, Sørensen S et al. (2011). Nitrogenase gene amplicons from global marine surface waters are dominated by genes of non-cyanobacteria. PLoS One 6: e19223.
16. Fernandez C, Farias L, Ulloa O. (2011). Nitrogen fixation in denitrified marine waters. PLoS One 6: 9.
17. Franz J, Krahmann G, Lavik G, Grasse P, Dittmar T, Riebesell U. (2012). Dynamics and stoichiometry of nutrients and phytoplankton in waters influenced by the oxygen minimum zone in the eastern tropical Pacific. Deep-Sea Res Pt I 62: 20-31.
18. Gandhi N, Singh A, Prakash S, Ramesh R, Raman M, Sheshshayee MS et al. (2011). First direct measurements of N2 fixation during a Trichodesmium bloom in the eastern Arabian Sea. Global Biogeochem Cycles 25: 10.
19. Grasshoff G, Kremling K, Erhardt M. (1999). Methods of Seawater Analysis. Wiley VCH: Weinheim, Germany.
20. Grosskopf T, LaRoche J. (2012). Direct and indirect costs of dinitrogen fixation in Crocosphaera watsonii WH8501 and possible implications for the nitrogen cycle. Front Aquat Microbiol 3: 236.
21. Grosskopf T, Mohr W, Baustian T, Schunck H, Gill D, Kuypers MMM et al. (2012). Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488: 361-364.
22. Halm H, Lam P, Ferdelman TG, Lavik G, Dittmar T, LaRoche J et al. (2012). Heterotrophic organisms dominate nitrogen fixation in the South Pacific Gyre. ISME J 6: 1238-1249.
23. Halm H, Musat N, Lam P, Langlois R, Musat F, Peduzzi S et al. (2009). Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ Microbiol 11: 1945-1958.
24. Hamersley MR, Turk KA, Leinweber A, Gruber N, Zehr JP, Gunderson T et al. (2011). Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight. Aquat Microb Ecol 63: 193.
25. Hong H, Kester DR. (1986). Redox state of iron in offshore waters of Peru. Limnol Oceanogr 31: 512-524.
26. Hutchins DA, Hare CE, Weaver RS, Zhang Y, Firme GF, DiTullio GR et al. (2002). Phytoplankton iron limitation in the Humboldt Current and Peru Upwelling. Limnol Oceanogr 47: 997-1011.
27. Ingall E, Jahnke R. (1994). Evidence for enhanced phosphorus regeneration from marine sediments overlain by oxygen depleted waters. Geochim Cosmochim Acta 58: 2571-2575.
28. Jayakumar A, Al-Rshaidat MMD, Ward BB, Mulholland MR. (2012). Diversity, distribution, and expression of diazotroph nifH genes in oxygen-deficient waters of the Arabian Sea. FEMS Microbiol Ecol 82: 597-606.
29. Kalvelage T, Lavik G, Lam P, Contreras S, Artega L, Löscher CR et al. (2013). Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nat Geosci 6: 228-234.
30. Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, Schubert CJ et al. (2007). Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 104: 7104-7109.
31. Lane BG, Bernier F, Dratewka-Kos E, Shafai R, Kennedy TD, Pyne C et al. (1991). Homologies between members of the germin gene family in hexaploid wheat and similarities between these wheat germins and certain Physarum spherulins. J Biol Chem 266: 10461-10469.
32. Langlois RJ, LaRoche J, Raab PA. (2005). Diazotrophic diversity and distribution in the tropical and subtropical Atlantic ocean. Appl Environ Microbiol 71: 7910-7919.
33. Langlois RJ, Hummer D, LaRoche J. (2008). Abundances and distributions of the dominant nifH phylotypes in the Northern Atlantic Ocean. Appl Environ Microbiol 74: 1922-1931.
34. Lavik G, Stuhrmann T, Bruchert V, Van der Plas A, Mohrholz V, Lam P et al. (2009). Detoxification of sulphidic African shelf waters by blooming chemolithotrophs. Nature 457: 581-U586.
35. Legendre P, Gallagher ED. (2001). Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.
36. Loescher CR, Kock A, Koenneke M, LaRoche J, Bange HW, Schmitz RA. (2012). Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosci Discuss 9: 2095-2122.
37. Mohr W, Grosskopf T, Wallace DWR, LaRoche J. (2010). Methodological underestimation of oceanic nitrogen fixation rates. PLoS One 5: e12583.
38. Montoya JP, Voss M, Kahler P, Capone DG. (1996). A simple, high-precision, high-sensitivity tracer assay for N2 fixation. Appl Environ Microbiol 62: 986-993.
39. Naqvi SWA, Jayakumar DA, Narveka PV, Naik H, Sarma VVSS, D'Souza W et al. (2000). Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408: 346-349.
40. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB et al. (2013). vegan: Community ecology package. R package version 2. 0-10. http://CRAN. R-project. org/package=vegan.
41. R Core Team. (2013). R: A language and environment for statistical computing. In: http://www. R-project. org/.
42. Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MMM et al. (2008). Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10: 3140-3149.
43. Schunck H, Lavik G, Desai DK, Grokopf T, Kalvelage T, Löscher CR et al. (2013). Giant hydrogen sulfide plume in the oxygen minimum zone off peru supports chemolithoautotrophy. PLoS One 8: e68661.
44. Stratil SB, Neulinger SC, Knecht H, Friedrichs AK, Wahl M. (2013). Temperature-driven shifts in the epibiotic bacterial community composition of the brown macroalga Fucus vesiculosus. Microbiologyopen 2: 338-349.
45. Turk KA, Rees AP, Zehr JP, Pereira N, Swift P, Shelley R et al. (2011). Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. ISME J 5: 1201-1212.
46. Ullrich W, Rigano C, Fuggi A, Aparicio P, Paneque A, Cejudo FJ et al. (1990). Nitrogen metabolism in heterotrophic bacteria. Simultaneous ammonia inhibition of nitrogen fixation and nitrate uptake and divalentation regulation of nitrate uptake in Azotobacter chroococcum. In Inorganic Nitrogen in Plants and Microorganisms. Springer: Berlin, Heidelberg, Germany, pp 93-98.
47. Zani S, Mellon MT, Collier JL, Zehr JP. (2000). Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Appl Environ Microbiol 66: 3119-3124.
48. Zehr JP, Turner PJ. (2001). Nitrogen fixation: nitrogenase genes and gene expression. In: Methods in Microbiology vol 30. Academic Press Inc: San Diego, CA, USA, pp 271-286.
49. Zehr JP, Mellon MT, Zani S. (1998). New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes (vol 64, pg 3444, 1998). Appl Environ Microbiol 64: 5067.
50. Zehr JP, Jenkins BD, Short SM, Steward GF. (2003). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5: 539-554.