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The contribution of denitrification and anaerobic ammonium oxidation to N2 production in mangrove sediments in Southeast China

  • Sediments, Sec 2 • Physical and Biogeochemical Processes • Research Article
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Abstract

Purpose

Mangrove forests, common in subtropical coastal regions, are known for their nitrogen (N) buffering capacity. The aims of this study were to examine temporal and spatial variations in denitrification and anaerobic ammonium oxidation (anammox) in mangrove sediments and to assess their contributions to nitrogen gas (N2) release.

Materials and methods

Cores of undisturbed mangrove sediments were collected during low tide. The potential anammox and denitrification rates were estimated by quantifying three forms of N2 produced in a strictly anaerobic incubation of sediment with labeled K15NO3 as the reactive substrate. Water samples from above the sediments were collected and analyzed for ammonium, nitrite, and nitrate concentrations.

Results and discussion

Denitrification and anammox were more active in summer. The contributions of anammox to total N2 in mangrove sediments were 42–70% (summer), 5–57% (autumn), and 26–43% (winter), respectively. There was no significant difference (P > 0.05) between seasons. Denitrification was the major mechanism of N loss overall; however, anammox was higher in the mangrove sediments in summer. Between 3.5 and 41.2% of dissolved inorganic nitrogen in the overlying water was converted to N2, which accounted for between 9 and 22% of the total N2 produced.

Conclusions

Denitrification and anammox operate simultaneously and make a significant contribution to the production and removal of N2 from mangrove systems. Denitrification was the major mechanism of N loss overall; however, anammox was not negligible in summer.

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References

  • Amano T, Yoshinaga I, Yamagishi T, Thuoc CV, Thu PT, Ueda S, Kato K, Sako Y, Suwa Y (2011) Contribution of anammox bacteria to benthic nitrogen cycling in a mangrove forest and shrimp ponds, Haiphong, Vietnam. Microbes Environ 26:1–6

    Article  Google Scholar 

  • Brin LD, Giblin AE, Rich JJ (2015) Effects of experimental warming and carbon addition on nitrate reduction and respiration in coastal sediments. Biogeochemistry 125:81–95

    Article  CAS  Google Scholar 

  • Chiu C-Y, Lee S-C, Chen T-H, Tian G (2004) Denitrification associated N loss in mangrove soil. Nutr Cycl Agroecosys 69:185–189

    Article  CAS  Google Scholar 

  • Dalsgaard T, Thamdrup B (2002) Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl Environ Microb 68:3802–3808

    Article  CAS  Google Scholar 

  • Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuña-González J (2003) N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422:606–608

    Article  CAS  Google Scholar 

  • Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464

    Article  CAS  Google Scholar 

  • Dittmar T, Lara RJ (2001) Do mangroves rather than rivers provide nutrients to coastal environments south of the Amazon River? Evidence from long-term flux measurements. Mar Ecol Prog Ser 213:67–77

    Article  CAS  Google Scholar 

  • Erler DV, Eyre BD, Davison L (2008) The contribution of anammox and denitrification to sediment N2 production in a surface flow constructed wetland. Environ Sci Technol 42:9144–9150

    Article  CAS  Google Scholar 

  • Fernandes SO, Michotey VD, Guasco S, Bonin PC, Bharathi PL (2012) Denitrification prevails over anammox in tropical mangrove sediments (Goa, India). Mar Environ Res 74:9–19

    Article  CAS  Google Scholar 

  • Hietanen S, Kuparinen J (2008) Seasonal and short-term variation in denitrification and anammox at a coastal station on the Gulf of Finland, Baltic Sea. Hydrobiologia 596:67–77

    Article  CAS  Google Scholar 

  • Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fert Soils 33:265–278

    Article  CAS  Google Scholar 

  • Hou L, Zheng Y, Liu M, Gong J, Zhang X, Yin G, You L (2013) Anaerobic ammonium oxidation (anammox) bacterial diversity, abundance, and activity in marsh sediments of the Yangtze Estuary. JGR-Biogeosciences 118:1237–1246

    CAS  Google Scholar 

  • Jensen MM, Kuypers MM, Gaute L, Thamdrup B (2008) Rates and regulation of anaerobic ammonium oxidation and denitrification in the Black Sea. Limnol Oceanogr 53:23–36

    Article  CAS  Google Scholar 

  • Jetten MS, Cirpus I, Kartal B, van Niftrik L, van de Pas-Schoonen KT, Sliekers O, Haaijer S, van der Star W, Schmid M, van de Vossenberg J, Schmidt I, Harhangi H, van Loosdrecht M, Gijs Kuenen J, Op den Camp H, Strous M (2005) 1994-2004: 10 years of research on the anaerobic oxidation of ammonium. Biochem Soc Trans 33:119–123

    Article  CAS  Google Scholar 

  • Koop-Jakobsen K, Giblin AE (2009) Anammox in tidal marsh sediments: the role of salinity, nitrogen loading, and marsh vegetation. Estuar Coasts 32:238–245

    Article  CAS  Google Scholar 

  • Kristensen E, Jensen MH, Banta GT, Hansen K, Holmer M, King GM (1998) Transformation and transport of inorganic nitrogen in sediments of a southeast Asian mangrove forest. Aquat Microb Ecol 15:165–175

    Article  Google Scholar 

  • Kuenzer C, Bluemel A, Gebhardt S, Quoc TV, Dech S (2011) Remote sensing of mangrove ecosystems: a review. Remote Sens 3:878–928

    Article  Google Scholar 

  • Kunu TM, Sullivan MB, Cornwell JC, Groxzkowski KM (1998) Denitrification in estuarine sediments determined by membrane inlet mass spectrometry. Limnol Oceanogr 43:334–339

    Article  Google Scholar 

  • Lawton J (2001) Earth system science. Science 292:1965–1965

    Article  CAS  Google Scholar 

  • Li H, Yang X, Zhang Z, Weng B, Huang F, Zhu G-B, Zhu Y-G (2015) Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. ISME J 9:2059–2067

    Article  Google Scholar 

  • Li M, Hong Y-G, Cao H-L, Gu J-D (2011) Mangrove trees affect the community structure and distribution of anammox bacteria at an anthropogenic-polluted mangrove in the Pearl River Delta reflected by 16S rRNA and hydrazine oxidoreductase (HZO) encoding gene analyses. Ecotoxicology 20:1780–1790

    Article  CAS  Google Scholar 

  • Meyer RL, Risgaard-Petersen N, Allen DE (2005) Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microb 71:6142–6149

    Article  CAS  Google Scholar 

  • Morell J, Corredor J (1993) Sediment nitrogen trapping in a mangrove lagoon. Estuar Coast Shelf S 37:203–212

    Article  CAS  Google Scholar 

  • Mulder A, Van de Graaf AA, Robertson L, Kuenen J (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16(3):177–183

    Article  CAS  Google Scholar 

  • Naeher S, Huguet A, Roose-Amsaleg CL, Laverman AM, Fosse C, Lehmann MF, Derenne S, Zopfi J (2015) Molecular and geochemical constraints on anaerobic ammonium oxidation (anammox) in a riparian zone of the Seine Estuary (France). Biogeochemistry 123:237–250

    Article  CAS  Google Scholar 

  • Nakajima J, Sakka M, Kimura T, Furukawa K, Sakka K (2008) Enrichment of anammox bacteria from marine environment for the construction of a bioremediation reactor. Appl Microbiol Bio 77:1159–1166

    Article  CAS  Google Scholar 

  • Nielsen LP (1992) Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiol Lett 86:357–362

    Article  CAS  Google Scholar 

  • Nielsen LP, Glud RN (1996) Denitrification in a coastal sediment measured in situ by the nitrogen isotope pairing technique applied to a benthic flux chamber. Mar Ecol Prog Ser 137:181–186

    Article  Google Scholar 

  • Oshiki M, Satoh H, Okabe S (2016) Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ Microbiol 18:2784–2796

    Article  CAS  Google Scholar 

  • Paredes D, Kuschk P, Köser H (2007) Influence of plants and organic matter on the nitrogen removal in laboratory-scale model subsurface flow constructed wetlands inoculated with anaerobic ammonium oxidizing bacteria. Eng Life Sci 7:565–576

    Article  CAS  Google Scholar 

  • Risgaard-Petersen N, Nielsen LP, Rysgaard S, Dalsgaard T, Meyer RL (2003) Application of the isotope pairing technique in sediments where anammox and denitrification coexist. Limnol Oceanogr-nMeth 1:63–73

    Article  Google Scholar 

  • Risgaard-Petersen N, Meyer RL, Revsbech NP (2005) Denitrification and anaerobic ammonium oxidation in sediments: effects of microphytobenthos and NO. Aquat Microb Eco 40:67–76

    Article  Google Scholar 

  • Rivera-Monroy VH, Twilley RR (1996) The relative role of denitrification and immobilization in the fate of inorganic nitrogen in mangrove sediments (Terminos Lagoon, Mexico). Limnol Oceanogr 41:284–296

    Article  CAS  Google Scholar 

  • Robertson A, Phillips M (1995) Mangroves as filters of shrimp pond effluent: predictions and biogeochemical research needs. Hydrobiologia 295:311–321

    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 

  • Stief P, Beer D, Neumann D (2002) Small-scale distribution of interstitial nitrite in freshwater sediment microcosms: the role of nitrate and oxygen availability, and sediment permeability. Microb Ecol 43:367–377

    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 Microb 68:1312–1318

    Article  CAS  Google Scholar 

  • Trimmer M, Nicholls JC, Deflandre B (2003) Anaerobic ammonium oxidation measured in sediments along the Thames estuary, United Kingdom. Appl Environ Microb 69:6447–6454

    Article  CAS  Google Scholar 

  • Wang M, Zhang J, Tu Z, Gao X, Wang W (2010) Maintenance of estuarine water quality by mangroves occurs during flood periods: a case study of a subtropical mangrove wetland. Mar Pollut Bull 60:2154–2160

    Article  CAS  Google Scholar 

  • Wu Y, Chung A, Tam N, Pi N, Wong M (2008) Constructed mangrove wetland as secondary treatment system for municipal wastewater. Ecol Eng 34:137–146

    Article  Google Scholar 

  • Zheng Y, Hou L, Liu M, Yin G, Gao J, Jiang X, Lin X, Li X, Yu C, Wang R (2016) Community composition and activity of anaerobic ammonium oxidation bacteria in the rhizosphere of salt-marsh grass Spartina alterniflora. Appl Microbiol Biot 100:1–10

    Article  Google Scholar 

  • Zhu G, Wang S, Feng X, Fan G, Jetten MS, Yin C (2011) Anammox bacterial abundance, biodiversity and activity in a constructed wetland. Environ Sci Technol 45:9951–9958

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the funding for this study from the National Basic Research Program of China through grant 2013CB956101 and Natural Science Foundation of China (41175130). We would also like to thank three reviewers for their valuable comments on the manuscript.

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Correspondence to Wenzhi Cao.

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Responsible editor: Haihan Zhang

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Cao, W., Guan, Q., Li, Y. et al. The contribution of denitrification and anaerobic ammonium oxidation to N2 production in mangrove sediments in Southeast China. J Soils Sediments 17, 1767–1776 (2017). https://doi.org/10.1007/s11368-017-1653-0

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  • DOI: https://doi.org/10.1007/s11368-017-1653-0

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