Applied Microbiology and Biotechnology

, Volume 89, Issue 4, pp 1233–1241 | Cite as

Diversity and abundance of anammox bacterial community in the deep-ocean surface sediment from equatorial Pacific

Environmental Biotechnology

Abstract

The community structure and diversity of anaerobic ammonium oxidation (anammox) bacteria in the surface sediments of equatorial Pacific were investigated by phylogenic analysis of 16S rRNA and hydrazine oxidoreductase (hzo) genes and PCoA (principal coordinates analysis) statistical analysis. Results indicated that 16S rRNA and hzo sequences in the P2 (off the center of western Pacific warm pool) and P3 (in the eastern equatorial Pacific) sites all belong to the Candidatus “Scalindua”, the dominate anammox bacteria in the low-temperature marine environment proved by previous studies. However, in the P1 site (in center of warm pool of western Pacific), large part of 16S rRNA gene sequences formed a separated cluster. Meanwhile, hzo gene sequences from P1 sediment also grouped into a single cluster. PCoA analysis demonstrated that the anammox community structure in the P1 has significant geographical distributional difference from that of P2, P3, and other marine environments based on 16S rRNA and hzo genes. The abundances of anammox bacteria in surface sediments of equatorial Pacific were quantified by q-PCR analysis of hzo genes, which ranged from 3.98 × 103 to 1.17 × 104 copies g−1 dry sediments. These results suggested that a special anammox bacteria phylotypes exist in the surface sediment of the western Pacific warm pool, which adapted to the specific habitat and maybe involved in the nitrogen loss process from the fixed inventory in the habitat.

Keywords

Anammox 16S rRNA gene hzo gene Surface sediment Western pacific warm pool 

References

  1. 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
  2. Byrne N, Strous M, Crepeau V, Kartal B, Birrien JL, Schmid M, Lesongeur F, Schouten S, Jaeschke A, Jetten M, Prieur D, Godfroy A (2009) Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents. ISME J 3:117–123CrossRefGoogle Scholar
  3. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, Garrity GM, Tiedje JM (2005) The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 33:294–296CrossRefGoogle Scholar
  4. Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol 11:1194–1207CrossRefGoogle Scholar
  5. de Graaf V, Mulder AA, de Bruijn A, Jetten MS, Robertson LA, Kuenen JG (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 61:1246–1251Google Scholar
  6. Devol AH (2003) Nitrogen cycle—solution to a marine mystery. Nature 422:575–576CrossRefGoogle Scholar
  7. Engstrom P, Penton CR, Devol AH (2009) Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol Oceanogr 54:1643–1652CrossRefGoogle Scholar
  8. 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 1:19–27CrossRefGoogle Scholar
  9. Glud RN, Thamdrup B, Stahl H, Wenzhoefer F, Glud A, Nomaki H, Oguri K, Revsbech NP, Kitazato H (2009) Nitrogen cycling in a deep ocean margin sediment (Sagami Bay, Japan). Limnol Oceanogr 54:723–734CrossRefGoogle Scholar
  10. Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, Sinninghe Damsté JS, Krúger S, Graco M, Gutirréz D, Kuypers MMM (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52:923–933CrossRefGoogle Scholar
  11. Jaeschke A, Abbas B, Zabel M, Hopmans EC, Schouten S, Damste JSS (2010) Molecular evidence for anaerobic ammonium-oxidizing (anammox) bacteria in continental shelf and slope sediments off northwest Africa. Limnol Oceanogr 55:365–376CrossRefGoogle Scholar
  12. Jetten MS, Sliekers O, Kuypers M, Dalsgaard T, van Niftrik L, Cirpus I, van de Pas-Schoonen K, Lavik G, Thamdrup B, Le Paslier D, Op den Camp HJ, Hulth S, Nielsen LP, Abma W, Third K, Engstrom P, Kuenen JG, Jorgensen BB, Canfield DE, Sinninghe Damste JS, Revsbech NP, Fuerst J, Weissenbach J, Wagner M, Schmidt I, Schmid M, Strous M (2003) Anaerobic ammonium oxidation by marine and freshwater planctomycete-like bacteria. Appl Microbiol Biotechnol 63:107–114CrossRefGoogle Scholar
  13. Jetten MS, Niftrik LV, Strous M, Kartal B, Keltjens JT, Op den Camp HJ (2009) Biochemistry and molecular biology of anammox bacteria. Crit Rev Biochem Mol Biol 44:65–84Google Scholar
  14. Kartal B, Rattray J, van Niftrik LA, van de Vossenberg J, Schmid MC, Webb RI, Schouten S, Fuerst JA, Sinninghe Damsté J, Jetten MSM, Strous M (2007) Candidatus “Anammoxoglobus propionicus” gen. nov., sp. nov., a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30:39–49CrossRefGoogle Scholar
  15. Kartal B, van Niftrik L, Rattray J, van de Vossenberg JLCM, Schmid MC, Sinninghe Damsté J, Jetten MSM, Strous M (2008) Candidatus ‘Brocadia fulgida’: anautofuorescent anaerobic ammoniumoxidizing bacterium. FEMS Microbiol Ecol 63:46–55CrossRefGoogle Scholar
  16. Klotz MG, Schmid MC, Strous M, op den Camp HJ, Jetten MS, Hooper AB (2008) Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ Microbiol 10:3150–3163CrossRefGoogle Scholar
  17. Kuenen JG (2008) Anammox bacteria: from discovery to application. Nat Rev Microbiol 6:320–326Google Scholar
  18. Kuypers MM, Sliekers AO, Lavik G, Schmid M, Jorgensen BB, Sinninghe KJG, Damsté JS, Strous M, Jetten MS (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422:608–611CrossRefGoogle Scholar
  19. Kuypers MMM, Lavik G, Woebken D, Schmid M, Fuchs BM, Amann RB, Jørgensen B, Jetten MSM (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA 102:6478–6483CrossRefGoogle Scholar
  20. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten MS, Kuypers MM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106:4752–4757CrossRefGoogle Scholar
  21. Landry MR, Kirchman DL (2002) Microbial community structure andvariability in the tropical Pacific. Deep Sea Res II 49:2669–2693CrossRefGoogle Scholar
  22. Li M, Hong Y-G, 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 86:781–790CrossRefGoogle Scholar
  23. Lozupone C, Hamady M, Knight R (2006) UniFrac-an onlinetool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform 7:371–384CrossRefGoogle Scholar
  24. Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee S-T, Park Y-H (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10:3130–3139CrossRefGoogle Scholar
  25. Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microb Ecol 55:311–320CrossRefGoogle Scholar
  26. Risgaard-Petersen N, Meyer RL, Schmid M, Jetten MSM, Enrich-Prast A, Rysgaard S, Revsbech NP (2004) Anaerobic ammonium oxidation in an estuarine sediment. Aquat Microb Ecol 36:293–304CrossRefGoogle Scholar
  27. Rysgaard S, Glud RN (2004) Anaerobic N-2 production in Arctic sea ice. Limnol Oceanogr 49:86–94CrossRefGoogle Scholar
  28. Rysgaard S, Glud RN, Risgaard-Petersen N, Dalsgaard T (2004) Denitrification and anammox activity in Arctic marine sediments. Limnol Oceanogr 49:1493–1502CrossRefGoogle Scholar
  29. Schalk J, de Vries S, Kuenen JG, Jetten MS (2000) Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39:5405–5412CrossRefGoogle Scholar
  30. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506CrossRefGoogle Scholar
  31. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23:93–106Google Scholar
  32. Schmid M, Walsh K, Webb R, Rijpstra WI, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Damsté JS, Harris J, Shaw P, Jetten M, Strous M (2003) Candidatus “Scalindua brodae”, sp. nov., Candidatus “Scalindua wagneri”, sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 26:529–538CrossRefGoogle Scholar
  33. Schmid MC, Risgaard-Petersen N, van de Vossenberg J, Kuypers MMM, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol 9:1476–1484CrossRefGoogle Scholar
  34. Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MM, Pommerening-Roeser A, op den Camp HJM, Jetten MSM (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10:3140–3149CrossRefGoogle Scholar
  35. Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K, Fujii T (2007) Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl Environ Microbiol 73:1065–1072CrossRefGoogle Scholar
  36. Stott L, Poulsen C, Lund S, Thunell R (2002) Super ENSO and global climate oscillations at millennial time scales. Science 297:222–226CrossRefGoogle Scholar
  37. Strous M, Fuerst J, Kramer E, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature 400:446–449CrossRefGoogle Scholar
  38. Strous M, Pelletier E, Mangeno S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Sne B, Dutilh BE, Op den Camp HJM, van der Drift C, Cirpus KT, van de Pas-Schoonen I, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes H-W, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794CrossRefGoogle Scholar
  39. Tal Y, Watts JE, Schreier HJ (2005) Anaerobic ammonia-oxidizing bacteria and related activity in Baltimore inner harbor sediment. Appl Environ Microbiol 71:1816–1821CrossRefGoogle Scholar
  40. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–15969CrossRefGoogle Scholar
  41. Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 8:1312–1318CrossRefGoogle Scholar
  42. Trimmer M, Nicholls JC, Morley N, Davies CA, Aldridge J (2005) Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment. Appl Environ Microbiol 71:1923–1930CrossRefGoogle Scholar
  43. van Niftrik LA, Fuerst JA, Sinninghe-Damsté JS, Kuenen JG, Jetten MS, Strous M (2004) The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 233:7–13CrossRefGoogle Scholar
  44. Visser K, Thunell R, Stott L (2003) Magnitude and timing of temperature change in the indo-Pacific Warm Pool during deglaciation. Nature 421:152–155CrossRefGoogle Scholar
  45. Wang P, Wang F, Xu M, Xiao X (2004) Molecular phylogeny of methylotrophs in a deep-sea sediment from a tropical west Pacific Warm Pool. FEMS Microbiol Ecol 47:77–84CrossRefGoogle Scholar
  46. Ward BB, Devol AH, Rich JJ, Chang BX, Bulow SE, Naik H, Pratihary A, Jayakumar A (2009) Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461:78–81CrossRefGoogle Scholar
  47. Woebken D, Lam P, Kuypers MM, Naqvi SW, Kartal B, Strous M, Jetten MS, Fuchs BM, Amann R (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10:3106–3119CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Key Laboratory of Tropical Marine Environment Dynamics (LED)South China Sea Institute of Oceanography, Chinese Academy of SciencesGuangzhouChina
  2. 2.State Key Laboratory of Marine Environmental ScienceXiamen UniversityXiamenChina

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