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

Limnology and Oceanography

Volumn 57, Issue 3, 2012, Pages 711-726

  Michael Beman, J ^a   Popp, Brian N ^a   Alford, Susan E ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM; ARRAY; BACTERIUM; CONCENTRATION (COMPOSITION); EUPHOTIC ZONE; GENE EXPRESSION; ION; NITROGEN; NUCLEIC ACID; OXIDATION; OXYGEN; PHYTOPLANKTON; POLYMERASE CHAIN REACTION; RESOLUTION; WATER COLUMN;

GULF OF CALIFORNIA; PACIFIC OCEAN; PACIFIC OCEAN (TROPICAL);

ARCHAEA; BACTERIA (MICROORGANISMS); NITROSOMONADALES;

EID: 84862011740     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2012.57.3.0711     Document Type: Article

References (59)

1. Agogue, H., M. Brink, J. Dinasquet, and G. J. Herndl. 2008. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456: 788-791, doi:10.1038/nature07535
2. Beman, J. M., K. R. Arrigo, and P. A. Matson. 2005. Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean. Nature 434: 211-214, doi:10.1038/nature03370
3. Beman, J. M., B. N. Popp, and C. A. Francis. 2008. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J. 2: 429-441, doi:10.1038/ismej.2007.118
4. Beman, J. M., R. Sachdeva, and J. A. Fuhrman. 2010. Population ecology of nitrifying Archaea and Bacteria in the Southern California Bight. Environ. Microbiol. 12: 1282-1292, doi:10.1111/j.1462-2920.2010.02172.x
5. Beman, J. M., and others. 2011. Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc. Natl. Acad. Sci. USA 108: 208-213, doi:10.1073/pnas.1011053108
6. Brochier-Armanet, C., B. Boussau, S. Gribaldo, and P. Forterre. 2008. Mesophilic crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6: 245-252, doi:10.1038/nrmicro1852
7. Brown, M. V., and others. 2009. Microbial community structure in the North Pacific Ocean. ISME J. 3: 1374-1386, doi:10.1038/ismej.2009.86
8. Canfield, D. E., A. N. Glazer, and P. G. Falkowski. 2010a. The evolution and future of Earth's nitrogen cycle. Science 330: 192-196, doi:10.1126/science.1186120
9. Canfield, D. E., and others. 2010b. A cryptic sulfur cycle in oxygenminimum-zone waters off the Chilean coast. Science 330: 1375-1378, doi:10.1126/science.1196889
10. Church, M. J., B. Wai, D. M. Karl, and E. F. DeLong. 2010. Abundances of crenarchaeal amoA genes and transcripts in the Pacific Ocean. Environ. Microbiol. 12: 679-688, doi:10.1111/j.1462-2920.2009.02108.x
11. Dore, J. E., and D. M. Karl. 1996. Nitrification in the euphotic zone as a source of nitrite, nitrate and nitrous oxide at Station ALOHA. Limnol. Oceanogr. 41: 1619-1628, doi:10.4319/lo.1996.41.8.1619
12. Dore, J. E., B. N. Popp, D.M. Karl, and F. J. Sansone. 1998. A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters. Nature 396: 63-66, doi:10.1038/23921
13. Engelbrektson, A., V. Kunin, K. C. Wrighton, N. Zvenigorodsky, F. Chen, H. Ochman, and P. Hugenholtz. 2010. Experimental factors affecting PCR-based estimates of microbial species richness and evenness. ISME J 4: 642-647, doi:10.1038/ismej.2009.153
14. Eppley, R. W., and B. J. Peterson. 1979. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282: 677, doi:10.1038/282677a0
15. Francis, C. A., J. M. Beman, and M. M. M. Kuypers. 2007. New processes and players in the nitrogen cycle: The microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1: 19-27, doi:10.1038/ismej.2007.8
16. Francis, C. A., K. J. Roberts, J. M. Beman, A. E. Santoro, and B. B. Oakley. 2005. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl. Acad. Sci. USA102: 14683-14688, doi:10.1073/pnas.0506625102
17. Galand, P. E., E. O. Casamayor, D. L. Kirchman, and C. Lovejoy. 2009. Ecology of the rare microbial biosphere of the Arctic Ocean. Proc. Natl. Acad. Sci. USA 106: 22427-22432, doi:10.1073/pnas.0908284106
18. Gruber, N. 2011. Warming up, turning sour, losing breath: Ocean biogeochemistry under global change. Phil. Trans. R. Soc. A 369: 1980-1996, doi:10.1098/rsta.2011.0003
19. Hamady, M., J. J. Walker, J. K. Harris, N. J. Gold, and R. Knight. 2008. Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat. Methods 5: 235-237, doi:10.1038/nmeth.1184
20. Holmes, R. M., A. Aminot, R. Kérouel, B. A. Hooker, and B. J. Peterson. 1999. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish. Aquat. Sci. 56: 1801-1808.
21. Huse, S., J. Huber, H. Morrison, M. Sogin, and D. Welch. 2007. Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol. 8: R143, doi:10.1186/gb-2007-8-7-r143
22. Hutchins, D. A., M. R. Mulholland, and F. Fu. 2009. Nutrient cycles and marine microbes in a CO2-enriched ocean. Oceanography 22: 128-145, doi:10.5670/oceanog.2009.103
23. Kanda, J., E. A. Laws, T. Saino, and A. Hattori. 1987. An evaluation of isotope dilution effect from conventional data sets of 15N uptake experiments. J. Plankton Res. 9: 79-90, doi:10.1093/plankt/9.1.79
24. Karl, D. M., G. A. Knauer, J. H. Martin, and B. B. Ward. 1984. Bacterial chemolithotrophy in the ocean is associated with sinking particles. Nature 309: 54-56, doi:10.1038/309054a0
25. Karner, M. B., E. F. DeLong, and D. M. Karl. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409: 507-510, doi:10.1038/35054051
26. Keeling, R. F., A. Kö rtzinger, and N. Gruber. 2010. Ocean deoxygenation in a warming world. Annu. Rev. Mar. Sci. 2: 199-229, doi:10.1146/annurev.marine.010908.163855
27. Kö nneke, M., A. E. Bernhard, J. R. de la Torre, C. B. Walker, J. B. Waterbury, and D. A. Stahl. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546, doi:10.1038/nature03911
28. Konstantinidis, K. T., J. Braff, D.M. Karl, and E. F. DeLong. 2009. Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at Station ALOHAin the North Pacific Subtropical Gyre. Appl. Environ. Microbiol. 75: 5345-5355, doi:10.1128/AEM.00473-09
29. Kunin, V., A. Engelbrektson, H. Ochman, and P. Hugenholtz. 2010. Wrinkles in the rare biosphere: Pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. 12: 118-123, doi:10.1111/j.1462-2920.2009.02051.x
30. Lam, P., and others. 2007. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc. Natl. Acad. Sci. USA 104: 7104-7109, doi:10.1073/pnas.0611081104
31. Lam, P., and others. 2009. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc. Natl. Acad. Sci. USA 106: 4752-4757, doi:10.1073/pnas.0812444106
32. Lipschultz, F., S. C. Wofsy, B. B. Ward, L. A. Codispoti, G. E. Friederich, and J. W. Elkins. 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, doi:10.1016/0198-0149(90)90060-9
33. Lomas, M. W., and F. Lipschultz. 2006. Forming the primary nitrite maximum: nitrifiers or phytoplankton? Limnol. Oceanogr. 51: 2453-2467, doi:10.4319/lo.2006.51.5.2453
34. Martens-Habbena, W., P. M. Berube, H. Urakawa, J. R. DE LA Torre, and D. A. Stahl. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461: 976-979, doi:10.1038/nature08465
35. Mills, M. M., C. Ridame, M. Davey, J. La Roche, and R. J. Gelder. 2004. Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429: 292-294, doi:10.1038/nature02550
36. Mincer, T. J., M. J. Church, L. T. Taylor, C. M. Preston, D. M. Karl, and E. F. DeLong. 2007. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ. Microbiol. 9: 1162-1175, doi:10.1111/j.1462-2920.2007.01239.x
37. Molina, V., L. Belmar, and O. Ulloa. 2010. High diversity of ammonia-oxidizing archaea in permanent and seasonal oxygendeficient waters of the eastern South Pacific. Environ. Microbiol. 12: 2450-2465, doi:10.1111/j.1462-2920.2010.02218.x
38. Molina, V., and L. Farías. 2009. Aerobic ammonium oxidation in the oxycline and oxygen minimum zone of the eastern tropical South Pacific off northern Chile (,20uS). Deep-Sea Res. II 56: 1032-1041, doi:10.1016/j.dsr2.2008.09.006
39. Molina, V., O. Ulloa, L. Farias, H. Urrutia, S. Ramirez, P. Junier, and K. Witzel. 2007. Ammonia-oxidizing betaproteobacteria from the oxygen minimum zone off northern Chile. Appl. Environ. Microbiol. 73: 3547-3555, doi:10.1128/AEM.02275-06
40. Popp, B. N., F. J. Sansone, T. M. Rust, and D. A. Merritt. 1995. Determination of concentration and carbon isotopic composition of dissolved methane in sediments and nearshore waters. Anal. Chem. 67: 405-411, doi:10.1021/ac00098a028
41. Prahl, F. G., B. N. Popp, D.M. Karl, and M. A. Sparrow. 2005. Ecology and biogeochemistry of alkenone production at subtropical North Pacific Station ALOHA. Deep-Sea Res. I 52: 699-719, doi:10.1016/j.dsr.2004.12.001
42. Raven, J. A. 2009. Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquat. Microb. Ecol. 56: 177-192, doi:10.3354/ame01315
43. Rees, A. P., E. M. S. Woodward, and I. Joint. 2006. Concentrations and uptake of nitrate and ammonium in the Atlantic Ocean between 60uN and 50uS. Deep-Sea Res. II 53: 1649-1665, doi:10.1016/j.dsr2.2006.05.008
44. Rotthauwe, J. H., K. P. Witzel, and W. Liesack. 1997. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63: 4704-4712.
45. Santoro, A. E., K. L. Casciotti, and C. A. Francis. 2010. Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current. Environ. Microbiol. 12: 1989-2006, doi:10.1111/j.1462-2920.2010.02205.x
46. Schloss, P. D., and others. 2009. Introducing mothur: Opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75: 7537-7541, doi:10.1128/AEM.01541-09
47. Sigman, D. M., K. L. Casciotti, M. Andreani, C. Barford, M. Galanter, and J. K. Bö hlke. 2001. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal. Chem. 73: 4145-4153, doi:10.1021/ac010088e
48. Stewart, F. J., O. Ulloa, and E. F. DeLong. 2012. Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ. Microbiol. 14: 23-40, doi:10.1111/j.1462-2920.2010.02400.x
49. Strickland, J. H., and T. R. Parsons. 1972. A practical handbook of seawater analysis, 2nd ed. Fisheries Research Board.
50. Sutka, R. L., N. E. Ostrom, P. H. Ostrom, and M. S. Phanikumar. 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. Acta 68: 517-527, doi:10.1016/S0016-7037(03)00483-6
51. Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73: 5261-5267, doi:10.1128/AEM.00062-07
52. Wankel, S. D., C. Kendall, J. T. Pennington, F. P. Chavez, AND A. Paytan. 2007. Nitrification in the euphotic zone as evidenced by nitrate dual isotopic composition: Observations from Monterey Bay, California. Glob. Biogeochem. Cycles 21: GB2009, doi:10.1029/2006GB002723
53. Ward, B. B. 2008. Nitrification in marine systems, p. 199-262. In D. G. Capone, D. Bronk, M. Mulholland, and E. J. Carpenter [eds.], Nitrogen in the marine environment, 2nd ed. Academic.
54. Ward, B. B., H. E. Glover, and F. Lipschultz. 1989a. Chemoautotrophic activity and nitrification in the oxygen minimum zone off Peru. Deep-Sea Res. A 36: 1031-1051, doi:10.1016/0198-0149(89)90076-9
55. Ward, B. B., K. A. Kilpatrick, E. H. Renger, and R. W. Eppley. 1989b. Biological nitrogen cycling in the nitracline. Limnol. Oceanogr. 34: 493-513, doi:10.4319/lo.1989.34.3.0493
56. Ward, B. B., and O. C. Zafiriou. 1988. Nitrification and nitric oxide in the oxygen minimum of the eastern tropical North Pacific. Deep-Sea Res. A 35: 1127-1142, doi:10.1016/0198-0149(88)90005-2
57. Ward, B. B., and others. 2009. Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461: 78-81, doi:10.1038/nature08276
58. White, A. E., F. G. Prahl, R. M. Letelier, and B. N. Popp. 2007. Summer surface waters in the Gulf of California: Prime habitat for biological N2 fixation. Glob. Biogeochem. Cycles 21: GB2017, doi:10.1029/2006GB002779
59. Yool, A., A. P. Martin, C. Fernandez, and D. R. Clark. 2007. The significance of nitrification for oceanic new production. Nature 447: 999-1002, doi:10.1038/nature 05885