Nitrite oxidation in the upper water column and oxygen minimum zone of the eastern tropical North Pacific Ocean

ISME Journal

Volumn 7, Issue 11, 2013, Pages 2192-2205

  Beman, J Michael ^a   Leilei Shih, Joy ^b   Popp, Brian N ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

nitrification; nitrite oxidation; nitrospina; oxygen minimum zone; pyrosequencing

Indexed keywords

AMMONIA; NITRITE; NITROGEN; OXYGEN; RNA 16S; SEA WATER;

AMMONIA; DATA SET; DISSOLVED OXYGEN; NITRITE; OXIDATION; WATER COLUMN;

ARTICLE; BACTERIUM; BIODIVERSITY; CHEMISTRY; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PACIFIC OCEAN;

AMMONIA; BACTERIA; BIODIVERSITY; MOLECULAR SEQUENCE DATA; NITRITES; NITROGEN; OXIDATION-REDUCTION; OXYGEN; PACIFIC OCEAN; RNA, RIBOSOMAL, 16S; SEAWATER;

PACIFIC OCEAN; PACIFIC OCEAN (NORTH);

BACTERIA (MICROORGANISMS); NITROSPINA;

EID: 84886720409     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.96     Document Type: Article

References (63)

1. Beman JM, Popp BN, Alford SE. (2012). Quantification of ammonia oxidation rates and ammonia-oxidizing archaea and bacteria at high resolution in the Gulf of California and eastern tropical North Pacific Ocean. Limnol Oceanog 57: 711-726.
2. Beman JM, Popp BN, Francis CA. (2008). Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2: 429-441.
3. Beman JM, Sachdeva R, Fuhrman JA. (2010). Population ecology of nitrifying Archaea and bacteria in the Southern California Bight. Environ Microbiol 12: 1282-1292.
4. Bianchi M, Fosset C, Conan P. (1999). Nitrification rates in the NW Mediterranean Sea. Aquat Microb Ecol 17: 267-278.
5. Brown MV, Philip GK, Bunge JA, Smith MC, Bissett A, Lauro FM et al. (2009). Microbial community structure in the North Pacific ocean. ISME J 3: 1374-1386.
6. Brown MV, Schwalbach M, Hewson I, Fuhrman JA. (2005). Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity: development and application to a time series. Environ Microbiol 7: 1466-1479.
7. Carlson CA, Morris R, Parsons R, Treusch AH, Giovannoni SJ, Vergin K. (2009). Seasonal dynamics of SAR11 populations in the euphotic and mesopelagic zones of the northwestern Sargasso Sea. ISME J 3: 283-295.
8. Casciotti KL, McIlvin MR. (2007). Isotopic analyses of nitrate and nitrite from reference mixtures and application to Eastern Tropical North Pacific waters. Mar Chem 107: 184-201.
9. Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP. (2005). Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 71: 5362-5370.
10. Clark DR, Rees AP, Joint I. (2008). Ammonium regeneration and nitrification rates in the oligotrophic Atlantic Ocean: implications for new production estimates. Limnol Oceanog 53: 52-62.
11. Costa E, Pérez J, Kreft J. (2006). Why is metabolic labour divided in nitrification? Trends Microbiol 14: 213-219.
12. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al. (2006). Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069-5072.
13. Deutsch C, Brix H, Ito T, Frenzel H, Thompson L. (2011). Climate-forced variability of ocean hypoxia. Science 333: 336-339.
14. DeVries T, Deutsch C, Primeau F, Chang B, Devol A. (2012). Global rates of water-column denitrification derived from nitrogen gas measurements. Nature Geosci 5: 547-550.
15. Dick GJ, Tebo BM. (2010). Microbial diversity and biogeochemistry of the Guaymas Basin deep-sea hydrothermal plume. Environ Microbiol 12: 1334-1347.
16. Dore JE, Karl DM. (1996). Nitrification in the euphotic zone as a source of nitrite, nitrate and nitrous oxide at station ALOHA. Limnol Oceanogr 41: 1619-1628.
17. Dore JE, Popp BN, Karl DM, Sansone FJ. (1998). A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters. Nature 396: 63-66.
18. Engelbrektson A, Kunin V, Wrighton KC, Zvenigorodsky N, Chen F, Ochman H et al. (2010). Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J 4: 642-647.
19. Francis CA, Beman JM, Kuypers MMM. (2007). New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1: 19-27.
20. Fuchs BM, Woebken D, Zubkov MV, Burkill P, Amann R. (2005). Molecular identification of picoplankton populationsin contrasting waters of the Arabian Sea. Aquat Microb Ecol 39: 145-157.
21. Fuhrman JA. (2009). Microbial community structure and its functional implications. Nature 459: 193-199.
22. Füssel J, Lam P, Lavik G, Jensen MM, Holtappels M, Gunter M et al. (2012). Nitrite oxidation in the Namibian oxygen minimum zone. ISME J 6: 1200-1209.
23. Galand PE, Casamayor EO, Kirchman DL, Lovejoy C. (2009). Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci USA 106: 22427-22432.
24. Gilly WF, Beman JM, Litvin SY, Robison BH. (2013). Oceanographic and biological effects of shoaling of the oxygen minimum zone. Annu Rev Marine Sci 5: 393-420.
25. Graham DW, Knapp CW, Van Vleck ES, Bloor K, Lane TB, Graham CE. (2007). Experimental demonstration of chaotic instability in biological nitrification. ISME J 1: 385-393.
26. Granger J, Sigman DM. (2009). Removal of nitrite with sulfamic acid for nitrate N and O isotope analysis with the denitrifier method. Rapid Commun Mass Spectrom 23: 3753-3762.
27. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R. (2008). Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Meth 5: 235-237.
28. Holmes RM, Aminot A, Kérouel R, Hooker BA, Peterson BJ. (1999). A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J FIsh Aquat Sci 56: 1801-1808.
29. Huse S, Huber J, Morrison H, Sogin M, Welch D. (2007). Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8: R143.
30. Karner MB, DeLong EF, Karl DM. (2001). Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507-510.
31. Keeling RF, Körtzinger A, Gruber N. (2010). Ocean deoxygenation in a warming world. Ann Rev Mar Sci 2: 199-229.
32. 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.
33. Lam P, Kuypers MMM. (2011). Microbial nitrogen cycling processes in oxygen minimum Zones. Annu Rev Marine Sci 3: 317-345.
34. Lam P, Lavik G, Jensen MM, van dV, Schmid M, Woebken D et al. (2009). Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106: 4752-4757.
35. Lipschultz F, Wofsy SC, Ward BB, Codispoti LA, Frieder-ich GE, Elkins JW. (1990). Bacterial transformations of inorganic nitrogen in the oxygen-deficient waters of the Eastern Tropical South Pacific Ocean. Deep Sea Res A 37: 1513-1541.
36. Lomas MW, Lipschultz F. (2006). Forming the primary nitrite maximum: nitrifiers or phytoplankton? Limnol Oceanog 51: 2453-2467.
37. Ma Y, Zeng Y, Jiao N, Shi Y, Hong N. (2009). Vertical distribution and phylogenetic composition of bacteria in the Eastern Tropical North Pacific Ocean. Microbiol Res 164: 624-633.
38. Mills MM, Ridame C, Davey M, La Roche J, Gelder RJ. (2004). Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429: 292-294.
39. Mincer TJ, Church MJ, Taylor LT, Preston CM, Karl DM, DeLong EF. (2007). Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9: 1162-1175.
40. 15N tracer studies of the primary nitrite maximum. J Mar Res 39: 203-226.
41. Paulmier A, Ruiz-Pino D. (2009). Oxygen minimum zones (OMZs) in the modern ocean. Prog Oceanogr 80: 113-128.
42. Popp BN, Sansone FJ, Rust TM, Merritt DA. (1995). Determination of concentration and carbon isotopic composition of dissolved methane in sediments and nearshore waters. Anal Chem 67: 405-411.
43. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
44. Redmond MC, Valentine DL. (2012). Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc Natl Acad Sci USA 109: 20292-20297.
45. Rich VI, Pham VD, Eppley J, Shi Y, DeLong EF. (2011). Time-series analyses of Monterey Bay coastal microbial picoplankton using a 'genome proxy' microarray. Environ Microbiol 13: 116-134.
46. Santoro AE, Casciotti KL, Francis CA. (2010). Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ Microbiol 12: 1989-2006.
47. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
48. Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Böhlke JK. (2001). A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73: 4145-4153.
49. Stramma L, Johnson GC, Sprintall J, Mohrholz V. (2008). Expanding oxygen-minimum zones in the tropical oceans. Science 320: 655-658.
50. Strickland JH, Parsons TR. (1972). A Practical Handbook of Seawater Analysis. Fisheries Research Board of Canada: Ottawa: Ontario, Canada.
51. Sutka RL, Ostrom NE, Ostrom PH, Phanikumar MS. (2004). Stable nitrogen isotope dynamics of dissolved nitrate in a transect from the North Pacific subtropical gyre to the eastern tropical North Pacific. Geochim Cosmochim Ac 68: 517-527.
52. Swan BK, Martinez-Garcia M, Preston CM, Sczyrba A, Woyke T, Lamy D et al. (2011). Potential for chemo-lithoautotrophy among ubiquitous bacteria lineages in the dark ocean. Science 333: 1296-1300.
53. Thamdrup B, Dalsgaard T, Revsbech NP. (2012). Widespread functional anoxia in the oxygen minimum zone of the Eastern South Pacific. Deep Sea Res I: Oceanog Res Papers 65: 36-45.
54. Ulloa O, Canfield DE, DeLong EF, Letelier RM, Stewart FJ. (2012). Microbial oceanography of anoxic oxygen minimum zones. Proc Natl Acad Sci USA 109: 15996-16003.
55. Walsh DA, Zaikova E, Howes CG, Song YC, Wright JJ, Tringe SG et al. (2009). Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science 326: 578-582.
56. Ward BB. (1987). Nitrogen transformations in the Southern California Bight. Deep Sea Res A 34: 785-805.
57. Ward BB, Devol AH, Rich JJ, Chang BX, Bulow SE, Naik H et al. (2009). Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461: 78-81.
58. Ward BB, Glover HE, Lipschultz F. (1989a). Chemoauto-trophic activity and nitrification in the oxygen minimum zone off Peru. Deep Sea Res A 36: 1031-1051.
59. Ward BB, Kilpatrick KA, Renger EH, Eppley RW. (1989b). Biological nitrogen cycling in the nitracline. Limnol Oceanogr 34: 493-513.
60. Ward BB, Zafiriou OC. (1988). Nitrification and nitric oxide in the oxygen minimum of the eastern tropical North Pacific. Deep Sea Res A 35: 1127-1142.
61. Woebken D, Fuchs BM, Kuypers MMM, Amann R. (2007). Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73: 4648-4657.
62. Wright JJ, Konwar KM, Hallam SJ. (2012). Microbial ecology of expanding oxygen minimum zones. Nat Rev Micro 10: 381-394.
63. Yool A, Martin AP, Fernandez C, Clark DR. (2007). The significance of nitrification for oceanic new production. Nature 447: 999-1002.