Skip to main content

Advertisement

Log in

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

  • Environmental Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 57:384–393

    Article  CAS  Google Scholar 

  • 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 3:117–123

    Article  CAS  Google Scholar 

  • 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 33:294–296

    Article  Google Scholar 

  • Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol 11:1194–1207

    Article  CAS  Google Scholar 

  • 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 61:1246–1251

    Google Scholar 

  • Devol AH (2003) Nitrogen cycle—solution to a marine mystery. Nature 422:575–576

    Article  CAS  Google Scholar 

  • Engstrom P, Penton CR, Devol AH (2009) Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol Oceanogr 54:1643–1652

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 54:723–734

    Article  CAS  Google Scholar 

  • 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 52:923–933

    Article  CAS  Google Scholar 

  • 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 55:365–376

    Article  CAS  Google Scholar 

  • 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 63:107–114

    Article  CAS  Google Scholar 

  • 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 44:65–84

    CAS  Google Scholar 

  • 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 30:39–49

    Article  CAS  Google Scholar 

  • 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 63:46–55

    Article  CAS  Google Scholar 

  • 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 10:3150–3163

    Article  CAS  Google Scholar 

  • Kuenen JG (2008) Anammox bacteria: from discovery to application. Nat Rev Microbiol 6:320–326

    Google Scholar 

  • 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 422:608–611

    Article  CAS  Google Scholar 

  • 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 102:6478–6483

    Article  CAS  Google Scholar 

  • 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 106:4752–4757

    Article  CAS  Google Scholar 

  • Landry MR, Kirchman DL (2002) Microbial community structure andvariability in the tropical Pacific. Deep Sea Res II 49:2669–2693

    Article  Google Scholar 

  • 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 86:781–790

    Article  CAS  Google Scholar 

  • Lozupone C, Hamady M, Knight R (2006) UniFrac-an onlinetool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform 7:371–384

    Article  Google Scholar 

  • 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 10:3130–3139

    Article  CAS  Google Scholar 

  • Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microb Ecol 55:311–320

    Article  CAS  Google Scholar 

  • 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 36:293–304

    Article  Google Scholar 

  • Rysgaard S, Glud RN (2004) Anaerobic N-2 production in Arctic sea ice. Limnol Oceanogr 49:86–94

    Article  CAS  Google Scholar 

  • Rysgaard S, Glud RN, Risgaard-Petersen N, Dalsgaard T (2004) Denitrification and anammox activity in Arctic marine sediments. Limnol Oceanogr 49:1493–1502

    Article  CAS  Google Scholar 

  • Schalk J, de Vries S, Kuenen JG, Jetten MS (2000) Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39:5405–5412

    Article  CAS  Google Scholar 

  • Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  CAS  Google Scholar 

  • 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 23:93–106

    CAS  Google Scholar 

  • 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 26:529–538

    Article  CAS  Google Scholar 

  • 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 9:1476–1484

    Article  CAS  Google Scholar 

  • 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 10:3140–3149

    Article  CAS  Google Scholar 

  • 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 73:1065–1072

    Article  CAS  Google Scholar 

  • Stott L, Poulsen C, Lund S, Thunell R (2002) Super ENSO and global climate oscillations at millennial time scales. Science 297:222–226

    Article  CAS  Google Scholar 

  • 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 400:446–449

    Article  CAS  Google Scholar 

  • 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 440:790–794

    Article  Google Scholar 

  • Tal Y, Watts JE, Schreier HJ (2005) Anaerobic ammonia-oxidizing bacteria and related activity in Baltimore inner harbor sediment. Appl Environ Microbiol 71:1816–1821

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–15969

    Article  CAS  Google Scholar 

  • Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 8:1312–1318

    Article  Google Scholar 

  • 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 71:1923–1930

    Article  CAS  Google Scholar 

  • 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 233:7–13

    Article  Google Scholar 

  • Visser K, Thunell R, Stott L (2003) Magnitude and timing of temperature change in the indo-Pacific Warm Pool during deglaciation. Nature 421:152–155

    Article  CAS  Google Scholar 

  • 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 47:77–84

    Article  CAS  Google Scholar 

  • 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 461:78–81

    Article  CAS  Google Scholar 

  • 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 10:3106–3119

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by Knowledge Innovation Key Project of The Chinese Academy of Sciences (KZCX2-YW-QN207); National Natural Science Foundation of China (No.30800032, 41076095, and 40930847) and MEL Advanced Visiting Scholarship (MELRS0911).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yi-Guo Hong.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hong, YG., Yin, B. & Zheng, TL. Diversity and abundance of anammox bacterial community in the deep-ocean surface sediment from equatorial Pacific. Appl Microbiol Biotechnol 89, 1233–1241 (2011). https://doi.org/10.1007/s00253-010-2925-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-010-2925-4

Keywords

Navigation