Microbial community structure and productivity in the oxygen minimum zone of the eastern tropical North Pacific

Deep-Sea Research Part I: Oceanographic Research Papers

Volumn 66, Issue , 2012, Pages 77-89

  Podlaska, Agnieszka ^a   Wakeham, Stuart G ^b,d   Fanning, Kent A ^c   Taylor, Gordon T ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b SKIDAWAY INSTITUTE OF OCEANOGRAPHY   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anammox; Chemoautotrophy; Diploptene; Microbial community structure; Nitrification; Oxygen minimum zone

Indexed keywords

ANAMMOX; CHEMOAUTOTROPHY; DIPLOPTENE; MICROBIAL COMMUNITY STRUCTURES; OXYGEN MINIMUM ZONE;

AMINO ACIDS; AMMONIUM COMPOUNDS; DENITRIFICATION; FLUORESCENCE MICROSCOPY; MICROORGANISMS; NITRIFICATION; OCEAN HABITATS; OXIDATION; SOCIAL SCIENCES; WASTEWATER TREATMENT;

NITROGEN REMOVAL;

ABUNDANCE; AMMONIUM; BACTERIUM; BIOLOGICAL PRODUCTION; BIOMARKER; CHEMOAUTOTROPHY; COMMUNITY STRUCTURE; CONCENTRATION (COMPOSITION); DISSOLVED INORGANIC CARBON; MICROBIAL COMMUNITY; NITRATE; NITRIFICATION; OXYGEN MINIMUM LAYER; UPWELLING;

PACIFIC OCEAN; PACIFIC OCEAN (TROPICAL);

BACTERIA (MICROORGANISMS); CRENARCHAEOTA; PLANCTOMYCETES; PROTEOBACTERIA;

EID: 84861978077     PISSN: 09670637     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dsr.2012.04.002     Document Type: Article

References (74)

1. Amann R.I., Binder B.J., Olson R.J., Chisholm S.W., Devereux R., Stahl D.A. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 1990, 56:1919-1925.
2. Amann R., Snaidr J., Wagner M., Ludwig W., Schleifer K.H. In situ visualization of high genetic diversity in a natural microbial community. J. Bacteriol. 1996, 178:3496-3500.
3. Arrigo K.R. Marine microorganisms and global nutrient cycles. Nature 2005, 437:349-355.
4. Barros G.V., Martinelli L.A., Oliveira Novais T.M., Ometto J.P.H.B., Zuppi G.M. Stable isotopes of bulk organic matter to trace carbon and nitrogen dynamics in an estuarine ecosystem in Balbitonga Bay (Santa Catarina, Brazil). Sci. Tot. Env. 2010, 408:2226-2232.
5. Brochier-Armanet C., Boussau B., Gribaldo S., Forterre P. Mesophilic crenarchaeota: proposal for a third archael phylum, the Thaumarchaeota. Nature Rev. Microbiol. 2008, 6:245-252.
6. Cabello P., Roldan M.D., Moreno-Vivian, C.M.D. Nitrate reduction and the nitrogen cycle in archaea. Microbiol. 2004, 150:3527-3546.
7. Canfield D.E., Stewart F.J., Thamdrup B., De Brabandere L., Dalsgaard T., Delong E.F., Revsbech N.P., Ulloa O. A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science 2010, 330:1375-1378.
8. Codispoti L.A., Brandes J.A., Christensen J.P., Devol A.H., Naqvi S.W.A., Paerl S.W.A., Yoshinari, T.H.W. The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene?. Sci. Mar. 2001, 65:85-105.
9. -1 vs the concept of homeostasis in the fixed-nitrogen inventory. Geosciences 2007, 4:233-253.
10. Cottrell M.T., Kirchman D.L. Natural Assemblages of Marine Proteobacteria and Members of the Cytophaga-Flavobacter Cluster Consuming Low- and High-Molecular-Weight Dissolved Organic Matter. Appl. Environ. Microbiol. 2000, 66(4):1692-1697.
11. Daims H., Brühl A., Amann R., Schleifer K.H., Wagner M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: Development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 1999, 22:434-444.
12. 2 production by the anammox reaction in the anoxic water column of Golfo Dulce. Costa Rica. Nature 2003, 422:606-608.
13. Diaz R.J., Rosenberg R. Spreading dead zones and consequences for marine ecosystems. Science 2008, 321:926-929.
14. Elvert M., Whiticar M.J., Suess E. Diploptene in varved sediments of Saanich Inlet: indicator of increasing bacterial activity under anaerobic conditions during the Holocene. Mar. Geol. 2001, 174:371-383.
15. 2 distributions in the equatorial Pacific during the 1991-1992 ENSO event. Deep Sea Res. Part II 1995, 42(2-3):365-386.
16. Fiedler P.C., Talley L.D. Hydrography of the eastern tropical Pacific: A review. Prog. Oceanogr. 2006, 69:143-180.
17. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., Oakley B.B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. PNAS 2005, 102(41):14683-14688.
18. Freeman K.H., Wakeham S.G., Hayes J.M. Predictive isotopic biogeochemistry: hydrocarbons from anoxic marine basins. Compound Specific Isotope Analysis in Biogeochemistry and Petroleum Geochemistry. Organic Geochemistry 1994, 21:629-644.
19. Galán A., Molina V., Thamdrup B., Woebken D., Lavik G., Kuypers M.M.M., Ulloa O. Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile. Deep Sea Res. Part II 2009, 56(16):1021-1031.
20. Gordon, L.I., Jennings, J.C. Jr., Ross, A.A., Krest, J.M., 1993. A suggested Protocol For Continuous Flow Automated Analysis of Seawater Nutrients. WOCE Operations Manual. WHP office Report 90-1, WOCE report 77 No. 68/91, pp. 1-52.
21. Grasshoff K. Methods of Seawater Analysis 1976, Verlag Chemie, Weinheim, New York, pp.134-145.
22. Hayes J.M. Fractionation of carbon and hydrogen isotopes in biosynthetic processes. Rev. Mineral. Geochem. 2001, 43:225-277.
23. Hobbie J.E., Daley R.J., Jasper S. Use of nucleopore filters for counting bacteria by fluorescence microscopy. Appl. Environ. Microbiol. 1977, 33:1225-1228.
24. Kannenberg E.L., Poralla K. Hopanoid biosynthesis and function in bacteria. Naturwissenschaften 1999, 86:168-176.
25. Kalvelage T., Jensen M.M., Contreras S., Revsbech N.P., Lam P., Günter M., LaRoche J., Lavik G., Kuypers M.M.M. Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. PLoS ONE 2011, 6(12):e29299. 10.1371/journal.pone.0029299.
26. Keeling R.F., Körtzinger A., Gruber N. Ocean deoxygenation in a warming world. Ann. Rev. Mar. Sci. 2010, 2:199-229.
27. Kirchman D.L. Leucine incorporation as a measure of biomass production by heterotrophic bacteria. Handbook of methods in aquatic microbial ecology 1993, 509-512. Lewis, Boca Raton, Florida. P. Kemp, B.F. Sherr, E.B. Sherr, J.J. Cole (Eds.).
28. Kowalchuk G.A., Stephen J.R. Ammonia-oxidizing bacteria: A Model for Molecular Microbial Ecology. Annu. Rev. Microbiol. 2001, 55(1):485-529.
29. Könneke M., Bernhard A.E., de la Torre J.R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
30. Kuypers M.M.M., Sliekers A.O., Lavik G., Schmid M., Jørgensen B.B., Kuenen J.G., Damste J.S.S., Strous M., Jetten M.S.M. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 2003, 422:608-611.
31. Kuypers M.M.M., Lavik G., Woebken D., Schmid M., Fuchs B.M., Amann R., Jørgensen B.B., Jetten M.S.M. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. PNAS 2005, 102:6478-6483.
32. Lam P., Jensen M.M., Lavik G., McGinnis D.F., Müller B., Schubert C.J., Amann R., Thamdrup B., Kuypers M.M.M. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. PNAS 2007, 104(17):7104-7109.
33. Lam P., Lavik G., Jensen M.M., Van de Vossenberg J., Schmid M., Woebken D., Gutiérrez D., Amann R., Jetten M.S.M., Kuypers M.M.M. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. PNAS 2009, 106(12):4752-4757.
34. Lin X., Wakeham S.G., Putnam I.F., Astor Y.M., Scranton M.I., Chistoserdov A.Y., Taylor G.T. Comparison of vertical distributions of prokaryotic assemblages in the anoxic Cariaco Basin and Black Sea by use of fluorescence in situ hybridization. Appl. Environ. Microbiol. 2006, 72:2679-2690.
35. Lin X., Scranton M.I., Chistoserdov A.Y., Varela R., Taylor G.T. Spatiotemporal dynamics of bacterial populations in the anoxic Cariaco Basin. Limnol. Oceanogr. 2008, 53(1):37-51.
36. Manz W., Amann R., Ludwig W., Wagner M., Schleifer K.H Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst. Appl. Microbiol. 1992, 15:593-600.
37. McFadden B.A. The ribulose bisphosphate pathway of CO 2 fixation. Autotrophic Bacteria 1989, 351-364. Springer, New York, ite. H.G. Schlegel, B. Bowien (Eds.).
38. Mobarry B.K., Wagner M., Urbain V., Rittmann B.E., Stahl D.A. Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Appl. Environ. Microbiol. 1996, 62:2156-2162.
39. Molina V., Farías L., Eissler Y., Cuevas Luis Antonio, Escribano, R.C.E.M. Ammonium cycling under a strong oxygen gradient associated with the Oxygen Minimum Zone off northern Chile (~23°S). Mar. Ecol. Prog. Ser. 2005, 288:35-43.
40. Molina V., Farías L. Aerobic ammonium oxidation in the oxycline and oxygen minimum zone of the eastern tropical South Pacific off northern Chile (~20°S). Deep Sea Res. Part II 2009, 56(16):1032-1041.
41. Mulder A., van de Graaf A.A., Robertson L.A., Kuenen J.G. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. Microbiol. Ecol. 1995, 16:177-184.
42. Neef, A., 1997. Anwendung der in situ Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen. Doctoral Thesis. Technische Universität München.
43. Neef A., Amann R., Schlesner H., Schleifer K.H. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 1998, 144:3257-3266.
44. Nelson D.C., Jorgensen B.B., Revsbech N.P. Growth pattern and yield of a chemoautotrophic Beggiatoa sp. in oxygen-sulfide microgradients. Appl. Environ. Microbiol. 1986, 52:225-233.
45. Ourisson G., Rohmer M. Hopanoids 2. Biohopanoids: a novel class of bacterial lipids. Acc. Chem. Res. 1992, 25:403-408.
46. Paerl H.W., Pinckney J.L. A mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling. Microb Ecol. 1996, 31:225-247.
47. Paulmier A., Ruiz-Pino D. Oxygen minimum zones (OMZs) in the modern ocean. Prog. Oceanogr. 2009, 80:113-128.
48. Pernthaler A., Pernthaler J., Amann R. Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria. Appl. Environ. Microbiol. 2002, 68:3094-3101.
49. Pitcher A., Villanueva L., Hopmans E.C., Schouten S., Reichart G.-J., Sinninghe Damsté J.S. Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J. 2011, 5:1896-1904.
50. Qi H., Coplen T.B., Geilmann H., Brand W.A., Bohlke J.K. Two new organic reference materials for δ13C and δ15N measurements and a new value for the δ13C of NBS 22 oil. Rapid Commun. Mass Spectrom. 2004, 17:2483-2487.
51. Rabalais N.N., Daz R.J., Levin L.A, Turner R.E., Gilbert D., Zhang J. Dynamics and distribution of natural and human-caused coastal hypoxia. Biogeosciences 2010, 7:585-619.
52. Rohmer M.P., Bouvier-Nave P., Ourisson G. Distribution of hopanoid triterprenes in prokaryotes. J. Gen. Microbiol. 1984, 130:1137-1150.
53. Ruby E.G., Jannasch H.W., Deuser W.G. Fractionation of stable carbon isotopes during chemoautotrophic growth of sulfur-oxidizing bacteria. Appl. Environ. Microbiol. 1987, 53:1940-1943.
54. Rusch D.B., Halpern A.L., Sutton G., Heidelberg K.B., Williamson S., Yooseph S., Wu D., Eisen J.A., Hoffman J.M., Remington K., Beeson K., Tran B., Smith H., Baden-Tillson H., Stewart C., Thorpe J., Freeman J., Andrews-Pfannkoch C., Venter J.E., Li K., Kravitz S., Heidelberg J.F., Utterback T., Rogers Y.-H., Falcón L.I., Souza V., Bonilla-Rosso G., Eguiarte L.E., Karl D.M., Sathyendranath S., Platt T., Bermingham E., Gallardo V., Tamayo-Castillo G., Ferrari M.R., Strausberg R.L., Nealson K., Friedman R., Frazier M., Venter J.C. The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biol. 2007, 5:e77. 10.1371/journal.pbio.0050077.
55. Rush D., Wakeham S.G., Hopmans E.C., Schouten S., Sinninghe Damstè S.S.J. Biomarker evidence for anammox in the oxygen minimum zone of the Eastern Tropical North Pacific. Org. Geochem. 2012, 10.1016/j.orggeochem.2012.02.005.
56. Sakata S., Hayes J.M., Rohmer M., Hooper A.B., Seemann M. Stable carbon-isotopic compositions of lipids isolated from the ammonia-oxidizing chemoautotroph Nitrosomonas europaea. Org. Geochem. 2008, 39:1725-1734.
57. Schmid M., Walsh K., Webb R., Rijpstra W.I., van de Pas-Schoonen K., Verbrug-gen J.M., Hill T., Moffet B., Fuerst J., Schouten S., Sinninghe Damstè S.S.J., Harris J., Shaw P., Jetten M., Strous M. Candidatus "Scalindua brodae", sp. nov., Candidatus "Scalindua wagneri", sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol. 2003, 26:529-538.
58. Schouten S., Strous M., Kuypers M.M.M., Rijpstra W.I.C., Baas M., Schubert C.J., Jetten M.S.M., Sinninghe Damsté J.S. Stable carbon isotopic fractionations associated with inorganic carbon fixation by anaerobic ammonium-oxidizing bacteria Appl. Environ. Microbiol. 2004, 70:3785-3788.
59. Sinninghe Damsté J.S., Rijpstra W.I.C., Schouten S., Fuerst J.A., Jetten M.S.M., Strous M. The occurrence of hopanoids in planctomycetes: implications for the sedimentary biomarker record. Org. Geochem. 2004, 35:561-566.
60. Siyambalapitiya N., Blackall L.L. Discrepancies in the widely applied GAM42a flourescence in situ hybridisation probe for Gammaproteobacteria. FEMS Microbiol. Lett. 2004, 242:367-373.
61. Stramma L., Johnson G.C., Sprintall J., Mohrholz V. Expanding oxygen minimum zones in the tropic oceans. Science 2008, 320:655-658.
62. Taylor G.T., Iabichella M., Ho T.Y., Scranton M.I., Thunell R.C., Muller-Karger F., Varela R. Chemoautotrophy in the Redox Transition Zone of the Cariaco Basin: A Significant Midwater Source of Organic Carbon Production. Limnol. Oceanogr. 2001, 46:148-163.
63. Teira E., Reinthaler T., Pernthaler A., Pernthaler J., Herndl G.J. Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by Bacteria and Archaea in the deep ocean. Appl. Environ. Microbiol. 2004, 70:4411-4414.
64. Thamdrup B., Dalsgaard T. Nitrogen cycling in sediments. Microbial ecology of the oceans 2008, 527-568. John Wiley and Sons, New Jersey. D.L. Kirchman (Ed.).
65. Tiedje J.M. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. Biology of Anaerobic Microorganisms 1988, 179-244. John Wiley and Sons, New York. A. Zehuder (Ed.).
66. 2O emissions. Appl. Environ. Microbiol. 1990, 56(6):1799-1805.
67. Van de Graaf A., Mulder A., De Brujin P., Jetten M.S.M., Robertson L.A., Kuenen J.G. Anaerobic Oxidation of Ammonium Is a Biologically Mediated Process. Appl. Environ. Microbiol. 1995, 61:1246-1251.
68. Wallner G., Amann R., Beisker W. Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 1993, 14:136-143.
69. Ward B., Zafiriou O. Nitrification and nitric oxide in the oxygen minimum of the eastern tropical North Pacific. Deep Sea Res. Part A. Oceanogr. Res. 1988, Papers 35(7):1127-1142.
70. Ward B., Glover H., Lipschultz F. Chemoautotrophic activity and nitrification in the oxygen minimum zone off Peru. Deep Sea Res. Part A. Oceanogr. Res. 1989, Papers 36(7):1031-1051.
71. Ward B.B., Tuit C.B., Jayakumar A., Rich J.J., Moffett J., Naqvi S.W.A. Organic carbon, and not copper, controls denitrification in oxygen minimum zones of the ocean. Deep Sea Res. I 2008, 55:1672-1683.
72. Wishner K.F., Ashjian C.J., Gelfman C., Gowing M.M., Kann L., Levin L.A., Mullineaux L.S., Saltzman J. Pelagic and benthic ecology of the lower interface of the Eastern Tropical Pacific oxygen minimum zone. Deep Sea Res. Part A. Oceanogr. Res. 1995, Papers 42:93-115.
73. Woebken D., Fuchs B.M., Kuypers M.M., Amann R. Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl. Environ. Microbiol. 2007, 73(14):4648-4657.
74. Wuchter C., Abbas B., Coolen M.J.C., Herfort L., van Bleijswijk J., Timmers P., Strous M., Teira E., Herndl G.J., Middelburg J.J., Schouten S., Sinninghe Damste J.S. Archaeal nitrification in the ocean. PNAS 2006, 103:12317-12322.