Microbial Ecology

, Volume 70, Issue 2, pp 311–321 | Cite as

Marine Oxygen-Deficient Zones Harbor Depauperate Denitrifying Communities Compared to Novel Genetic Diversity in Coastal Sediments

  • Jennifer L. Bowen
  • David Weisman
  • Michie Yasuda
  • Amal Jayakumar
  • Hilary G. Morrison
  • Bess B. Ward
Microbiology of Aquatic Systems
First Online:
Received:
Accepted:

Abstract

Denitrification is a critically important biogeochemical pathway that removes fixed nitrogen from ecosystems and thus ultimately controls the rate of primary production in nitrogen-limited systems. We examined the community structure of bacteria containing the nirS gene, a signature gene in the denitrification pathway, from estuarine and salt marsh sediments and from the water column of two of the world’s largest marine oxygen-deficient zones (ODZs). We generated over 125,000 nirS gene sequences, revealing a large degree of genetic diversity including 1,815 unique taxa, the vast majority of which formed clades that contain no cultured representatives. These results underscore how little we know about the genetic diversity of metabolisms underlying this critical biogeochemical pathway. Marine sediments yielded 1,776 unique taxa when clustered at 95 % sequence identity, and there was no single nirS denitrifier that was a competitive dominant; different samples had different highly abundant taxa. By contrast, there were only 39 unique taxa identified in samples from the two ODZs, and 99 % of the sequences belonged to 5 or fewer taxa. The ODZ samples were often dominated by nirS sequences that shared a 92 % sequence identity to a nirS found in the anaerobic ammonium-oxidizing (anammox) genus Scalindua. This sequence was abundant in both ODZs, accounting for 38 and 59 % of all sequences, but it was virtually absent in marine sediments. Our data indicate that ODZs are remarkably depauperate in nirS genes compared to the remarkable genetic richness found in coastal sediments.

Keywords

Anammox Denitrification Estuarine sediments Nitrite reductase (nirS) Oxygen-deficient zones Salt marshes 
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Notes

Acknowledgments

Funding for this work came from multiple NSF grants to BBW and from the following NSF grants: DEB-0717155 (to John Hobbie) and DBI-0400819 (to Jennifer L. Bowen). Additional support was provided via start-up funds from University of Massachusetts Boston to JLB. We would like to acknowledge the Salt Pond Sanctuaries and Dr. E. F. X. Hughes and family for allowing us to have access to the Great Sippewissett marsh plots, and Ivan Valiela for providing support and maintenance of the plots. Christopher Jones and Sara Hallin provided us with their curated nirS alignment. Comments from anonymous reviewers greatly improved the quality of this manuscript.

Supplementary material

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References

  1. 1.
    Galloway JN, Dentener JF, Capone DG, Boyer EW, Howarth RW, Seitzinger SP et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  2. 2.
    Thamdrup B (2012) New pathways and processes in the global nitrogen cycle. Ann Rev Ecol Evol Syst 43:407–428CrossRefGoogle Scholar
  3. 3.
    Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  4. 4.
    Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of earth’s nitrogen cycle. Science 330:192–196PubMedCrossRefGoogle Scholar
  5. 5.
    Smil V (2002) Nitrogen and food production: proteins for human diets. Ambio 31:126–131PubMedGoogle Scholar
  6. 6.
    Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Crosby BJ (2003) The nitrogen cascade. Bioscience 53:341–356CrossRefGoogle Scholar
  7. 7.
    Bricker SB, Longstaff B, Dennison W, Jones A, Boicourt K, Wicks C et al (2008) Effects of nutrient enrichment in the nation’s estuaries: a decade of change. Harmful Algae 8:21–32CrossRefGoogle Scholar
  8. 8.
    Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929PubMedCrossRefGoogle Scholar
  9. 9.
    Zumft W (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616PubMedCentralPubMedGoogle Scholar
  10. 10.
    Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jørgensen BB, Kuenen JG et al (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422:608–611PubMedCrossRefGoogle Scholar
  11. 11.
    Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann R et al (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci U S A 102:6239–6240CrossRefGoogle Scholar
  12. 12.
    Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D et al (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci U S A 106:4752–4757PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Lam P, Kuypers MMM (2011) Microbial nitrogen cycling processes in oxygen minimum zones. Ann Rev Mar Sci 3:317–345PubMedCrossRefGoogle Scholar
  14. 14.
    Codispoti LA, Brandes JA, Christensen JP, Devol AH, Naqvi SWA, Paerl HW et al (2001) The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene? Sci Mar 65:85–105CrossRefGoogle Scholar
  15. 15.
    Gruber N, Sarmiento JL (1997) Global patterns of marine nitrogen fixation and denitrification. Global Biogeochem Cy 11:235–266CrossRefGoogle Scholar
  16. 16.
    Hopkinson CS, Giblin AE (2008) Nitrogen dynamics of coastal salt marshes. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the Marine Environment, 2nd edn. Elsevier, Amsterdam, pp 991–1036CrossRefGoogle Scholar
  17. 17.
    Koop-Jakobsen K, Giblin AE (2009) Anammox in tidal marsh sediments: the role of salinity, nitrogen loading, and marsh vegetation. Estuar Coasts 32:238–245CrossRefGoogle Scholar
  18. 18.
    Koop-Jakobsen K, Giblin AE (2010) The effect of increased nitrate loading on nitrate reduction via denitrification and DNRA in salt marsh sediments. Limnol Oceanogr 55:789–802CrossRefGoogle Scholar
  19. 19.
    Hamersley MR, Howes BL (2005) Coupled nitrification–denitrification measured in situ in a Spartina alterniflora marsh with a 15NH4 tracer. Mar Ecol Prog Ser 299:123–135CrossRefGoogle Scholar
  20. 20.
    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 461:78–81PubMedCrossRefGoogle Scholar
  21. 21.
    Dalsgaard T, Thamdrup B, Farias L, Peter Revsbech NP (2012) Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnol Oceanogr 57:1331–1346CrossRefGoogle Scholar
  22. 22.
    Ward BB (2013) How nitrogen is lost. Science 341:352–353PubMedCrossRefGoogle Scholar
  23. 23.
    Zehr JP, Kudela RM (2011) Nitrogen cycle of the open ocean: from genes to ecosystems. Ann Rev Mar Sci 3:197–225PubMedCrossRefGoogle Scholar
  24. 24.
    Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4:633–641PubMedCrossRefGoogle Scholar
  25. 25.
    Abell GCJ, Revill AT, Smith C, Bissett AP, Volkman JK, Robert SS (2009) Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary. ISME J 4:286–300PubMedCrossRefGoogle Scholar
  26. 26.
    Nogales B, Timmis KN, Nedwell DB, Osborne AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl Environ Microbiol 68:5017–5025PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW et al (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794PubMedCrossRefGoogle Scholar
  28. 28.
    Schmid MC, Maas B, Dapena A, van de Pas-Schoonen K, Van De Vossenberg J, Kartal B et al (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microb 71:1677–1684CrossRefGoogle Scholar
  29. 29.
    Li M, Hong Y, Klotz MG, Gu J-D (2010) A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments. Appl Microbiol Biotechnol 86:781–790PubMedCrossRefGoogle Scholar
  30. 30.
    Li M, Ford T, Li X, Gu J-D (2011) Cytochrome cd1-containing nitrite reductase encoding gene nirS as a new functional biomarker for detection of anaerobic ammonium oxidizing (anammox) bacteria. Environ Sci Technol 45:3547–3553PubMedCrossRefGoogle Scholar
  31. 31.
    Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR et al (2006) Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci U S A 103:12115–12120PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ et al (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Nat Acad Sci USA 108:4516–4522PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Canfield DE, Stewart FJ, Thamdrup B, Brabandere LD, Dalsgaard T, Delong EF et al (2010) A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 330:1375–1378PubMedCrossRefGoogle Scholar
  34. 34.
    Stewart FJ, Ulloa O, Delong EF (2012) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol 14:23–40PubMedCrossRefGoogle Scholar
  35. 35.
    Ulloa O, Canfield DE, Delong EF, Letelier RM, Stewart FJ (2012) Microbial oceanography of anoxic oxygen minimum zones. Proc Natl Acad Sci U S A 109:15996–16003PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Gifford SM, Sharma S, Rinta-Kanto JM, Moran MA (2010) Quantitative analysis of a deeply sequenced marine microbial metatranscriptome. ISME J 5:461–472PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Penton CR, Johnson TA, Quensen JF III, Iwai S, Cole JR, Tiedje JM (2013) Functional genes to assess nitrogen cycling and aromatic hydrocarbon degradation: primers and processing matter. Front Microbiol 4:279PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Palmer K, Biasi C, Horn MA (2012) Contrasting denitrifier communities relate to contrasting N2O emission pattern from acidic peat soils in arctic tundra. ISME J 6:1058–1077PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Dumont MG, Lüke C, Deng Y, Frenzel P (2014) Classification of pmoA amplicon pyrosequences using BLAST and the lowest common ancestor method in MEGAN. Front Microbiol 5:34PubMedCentralCrossRefGoogle Scholar
  40. 40.
    Francis CA, O’Mullan GD, Ward BB (2003) Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1:129–140CrossRefGoogle Scholar
  41. 41.
    Bulow SE, Francis CA, Jackson GA, Ward BB (2008) Sediment denitrifier community composition and nirS gene expression investigated with functional gene microarrays. Environ Microbiol 10:3057–3069PubMedCrossRefGoogle Scholar
  42. 42.
    Valiela I, Teal JM, Persson NY (1976) Production and dynamics of experimentally enriched salt marsh vegetation: belowground biomass. Limnol Oceanogr 21:245–252CrossRefGoogle Scholar
  43. 43.
    Valiela I, Teal JM, Sass WJ (1975) Production and dynamics of salt marsh vegetation and the effects of experimental treatment with sewage sludge: biomass, production and species composition. J Appl Ecol 12:973–981CrossRefGoogle Scholar
  44. 44.
    Bowen JL, Byrnes JEK, Weisman D, Colaneri C (2013) Functional gene pyrosequencing and network analysis: an approach to examine the response of denitrifying bacteria to increased nitrogen supply in salt marsh sediments. Front Microbiol 342:1–12Google Scholar
  45. 45.
    Jayakumar A, O’Mullan GD, Naqvi SWA, Ward BB (2009) Denitrifying bacterial community composition changes associated with stages of denitrification in oxygen minimum zones. Microb Ecol 58:350–362PubMedCrossRefGoogle Scholar
  46. 46.
    Weisman D, Yasuda M, Bowen JL (2013) FunFrame: Functional gene ecological analysis pipeline. Bioinformatics 29:1212–1214PubMedCrossRefGoogle Scholar
  47. 47.
    Braker G, Fesefeldt A, Witzel KP (1998) Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microb 64:3769–3775Google Scholar
  48. 48.
    Quince C, Lanzén A, Curtis TP, Davenport RJ, Hall N, Head IM et al (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6:639PubMedCrossRefGoogle Scholar
  49. 49.
    Kunin V, Engelbrektson A, Ochman H, Hugenholtz P (2010) Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 12:118–123PubMedCrossRefGoogle Scholar
  50. 50.
    Quince C, Lanzén A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinf 12:38CrossRefGoogle Scholar
  51. 51.
    Schloss PD, Westcott SL (2011) Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol 77:3219–3226PubMedCentralPubMedCrossRefGoogle Scholar
  52. 52.
    Zhang Y, Sun Y (2011) HMM-FRAME: accurate protein domain classification for metagenomic sequences containing frameshift errors. BMC Bioinformatics 12:198PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Cock PJA, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A et al (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25:1422–1423PubMedCentralPubMedCrossRefGoogle Scholar
  55. 55.
    Francis CA, O’Mullan GD, Cornwell JC, Ward BB (2013) Transitions in nirS-type denitrifier diversity, community composition, and biogeochemical activity along the Chesapeake Bay estuary. Front Microbiol 237:1–10Google Scholar
  56. 56.
    Cai Y, Sun Y (2011) ESPRIT-Tree: hierarchical clustering analysis of millions of 16S rRNA pyrosequences in quasilinear computational time. Nucleic Acids Res 39:e95–e95PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Gihring TM, Green SJ, Schadt CW (2011) Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environ Microbiol 14:285–290PubMedCrossRefGoogle Scholar
  59. 59.
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin, O’Hara RB, et al (2013) Vegan: community ecology package. R package version 2.0-7. http://cran.r-project.org/web/packages/vegan/
  60. 60.
    R. Core Team (2014) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  61. 61.
    Caporaso JG, Bittinger K, Bushman FD, Desantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Price MN, Dehal PS, Arkin AP (2010) FastTree 2: approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Letunic I, Bork P (2011) Interactive tree of life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Stevens H, Ulloa O (2008) Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ Microbiol 10:1244–1259PubMedCrossRefGoogle Scholar
  65. 65.
    Bryant JA, Stewart FJ, Eppley JM, Delong EF (2012) Microbial community phylogenetic and trait diversity declines with depth in a marine oxygen minimum zone. Ecology 93:1659–1673PubMedCrossRefGoogle Scholar
  66. 66.
    Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 104:11436–11440PubMedCentralPubMedCrossRefGoogle Scholar
  67. 67.
    Bowen JL, Morrison HG, Hobbie JE, Sogin ML (2012) Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates. ISME J 6:2014–2023PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    Kondo R, Purdy KJ, Silva SQ, Nedwell DB (2007) Spatial dynamics of sulphate-reducing bacterial compositions in sediment along a salinity gradient in a UK Estuary. Microbes Environ 22:11–19CrossRefGoogle Scholar
  69. 69.
    Klepac-Ceraj V, Bahr M, Crump BC, Teske AP, Hobbie JE, Polz MF (2004) High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria. Environ Microbiol 6:686–698PubMedCrossRefGoogle Scholar
  70. 70.
    Bahr M, Crump BC, Klepac-Ceraj V, Teske A, Sogin ML, Hobbie JE (2005) Molecular characterization of sulfate-reducing bacteria in a New England salt marsh. Environ Microbiol 7:1175–1185PubMedCrossRefGoogle Scholar
  71. 71.
    Beman JM, Francis CA (2006) Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahia del Tobari, Mexico. Appl Environ Microbiol 72:7767–7777PubMedCentralPubMedCrossRefGoogle Scholar
  72. 72.
    Mosier AC, Francis CA (2008) Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environ Microbiol 10:3002–3016PubMedCrossRefGoogle Scholar
  73. 73.
    Moin NS, Nelson KA, Bush A, Bernhard AE (2009) Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Appl Environ Microb 75:7461–7468CrossRefGoogle Scholar
  74. 74.
    Lovell CR, Friez MJ, Longshore JW, Bagwell CE (2001) Recovery and phylogenetic analysis of nifH sequences from diazotrophic bacteria associated with dead aboveground biomass of Spartina alterniflora. Appl Environ Microbiol 67:5308–5314PubMedCentralPubMedCrossRefGoogle Scholar
  75. 75.
    Bagwell CE, Dantzler M, Bergholz PW, Lovell CR (2001) Host-specific ecotype diversity of rhizoplane diazotrophs of the perennial glasswort Salicornia virginica and selected salt marsh grasses. Aquat Microb Ecol 23:293–300CrossRefGoogle Scholar
  76. 76.
    Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554PubMedCrossRefGoogle Scholar
  77. 77.
    Lehmann J, Solomon D, Kinyangi J, Dathe L, Wirick S, Jacobsen C (2008) Spatial complexity of soil organic matter forms at nanometre scales. Nat Geosci 1:238–242CrossRefGoogle Scholar
  78. 78.
    Howes BL, Howarth RW, Teal JM, Valiela I (1981) Oxidation–reduction potentials in a salt marsh: spatial patterns and interactions with primary production. Limnol Oceanogr 26:350–360CrossRefGoogle Scholar
  79. 79.
    Crump BC, Hopkinson CS, Sogin ML, Hobbie JE (2004) Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Appl Environ Microbiol 70:1494–1505PubMedCentralPubMedCrossRefGoogle Scholar
  80. 80.
    Woebken D, Lam P, Kuypers MMM, Naqvi SWA, Kartal B et al (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10:3106–3119PubMedCrossRefGoogle Scholar
  81. 81.
    Jayakumar A, Naqvi SWA, Ward BB (2009) Distribution and relative quantification of key genes involved in fixed nitrogen loss from the Arabian Sea oxygen minimum zone. In: Wiggert JD, Hood RR, Naqvi SWA, Brink KH, Smith SL (eds) Indian ocean biogeochemical processes and ecological variability. American Geophysical Union, Washington, DC, pp 187–203Google Scholar
  82. 82.
    Jayakumar DA, Francis CA, Naqvi SWA, Ward BB (2004) Diversity of nitrite reductase genes (nirS) in the denitrifying water column of the coastal Arabian Sea. Aquat Microb Ecol 34:69–78CrossRefGoogle Scholar
  83. 83.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235PubMedCentralPubMedCrossRefGoogle Scholar
  84. 84.
    Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172PubMedCentralPubMedCrossRefGoogle Scholar
  85. 85.
    Jayakumar A, Peng X, Ward BB (2013) Community composition of bacteria involved in fixed nitrogen loss in the water column of two major oxygen minimum zones in the ocean. Aquat Microb Ecol 70:245–259CrossRefGoogle Scholar
  86. 86.
    Thamdrup B, Dalsgaard T, Jensen MM, Ulloa O, Farias L, Escribano R (2006) Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnol Oceanogr 51:2145–2156CrossRefGoogle Scholar
  87. 87.
    Bulow SE, Rich JJ, Naik HS, Pratihary AK, Ward BB (2010) Denitrification exceeds anammox as a nitrogen loss pathway in the Arabian Sea oxygen minimum zone. Deep-Sea Res I 57:384–393CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Jennifer L. Bowen
    • 1
  • David Weisman
    • 1
  • Michie Yasuda
    • 1
  • Amal Jayakumar
    • 3
  • Hilary G. Morrison
    • 2
  • Bess B. Ward
    • 3
  1. 1.Department of BiologyUniversity of MassachusettsBostonUSA
  2. 2.Josephine Bay Paul Center for Comparative Molecular Biology and EvolutionMarine Biological LaboratoryWoods HoleUSA
  3. 3.Department of GeosciencesPrinceton UniversityPrincetonUSA

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