An overlooked nitrogen loss linked to anaerobic ammonium oxidation in estuarine sediments in China
Despite its importance, anammox (anaerobic ammonium oxidation) in estuarine sediment systems remains poorly understood, particularly at the continental scale. This study aimed to understand the abundance, diversity, and activity of anammox bacteria and to determine the main factors influencing the anammox process in estuarine sediments in China.
Materials and methods
Estuarine sediments were collected from 18 estuaries spanning over 4000 km. Experiments using an 15 N–tracer, quantitative PCR, and clone library construction were used to determine the activity, abundance, and diversity of anammox bacteria. The impact of environmental factors on anammox processes was also determined.
Results and discussion
The abundance of the anammox-specific hydrazine synthase (hzsB) gene ranged from 1.8 × 105 ± 3.4 × 104 to 3.6 × 108 ± 7.5 × 107 copies g−1 dw. Candidatus Scalindua, Brocadia, Kuenenia, Jettenia, and two novel unidentified clusters were detected, with Scalindua dominating the anammox population. Additionally, the abundances of Scalindua, Kuenenia, and Brocadia were found to be significantly correlated with latitude. The anammox rates ranged from 0.29 ± 0.15 to 13.68 ± 3.98 nmol N g−1 dw h−1 and contributed to 2.39–82.61% of total N2 production. Pearson correlation analysis revealed that the anammox rate was positively correlated with total nitrogen, total carbon, and temperature, and was negatively correlated with dissolved oxygen (DO). The key factors influencing the hzsB gene abundance were ammonium concentration, salinity, and DO. Ammonium concentration, pH, temperature, and latitude were main variables shaping the anammox-associated bacterial community.
Our results suggested that anammox bacteria are ubiquitous in coastal estuaries in China and underline the importance of anammox resulting in N loss at a continental scale.
KeywordsActivity Anammox Estuarine sediments N loss Spatial variation
This study was financially supported by the Natural Science Foundation of China (41401297, 41571130063), the China Postdoctoral Science Foundation (2014M551846), and the International Science & Technology Cooperation Program of China (2011DFB91710).
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Meth 7(5):335–336CrossRefGoogle Scholar
- China Agricultural Yearbook, 2012Google Scholar
- Jetten MSM, Op den Camp HJM, Kuenen JG, Strous M (2010) Description of the order Brocadiales. In: Krieg NR, Staley JT, Hedlund BP, Paster BJ, Ward N, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology. Springer, HeidelbergGoogle Scholar
- Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Roser A, Koops HP, Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64:3042–3051Google Scholar
- Li M, Hong YG, Cao HL, Gu JD (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 20:1780–1790CrossRefGoogle Scholar
- Richard FA (1965) Anoxic basins and fjords. In: Ripley JP, Skirrow G (eds) Chemical oceanography, vol 1. Academic Press, Manhattan, pp 611–645Google Scholar
- Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541CrossRefGoogle Scholar
- Schmid M, Walsh K, Webb R, Rijpstra WIC, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Damste JSS, 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
- Schmid MC, Maas B, Dapena A, de Pas-Schoonen KV, de Vossenberg JV, Kartal B, van Niftrik L, Schmidt I, Cirpus I, Kuenen JG, Wagner M, Damste JSS, Kuypers M, Revsbech NP, Mendez R, Jetten MSM, Strous M (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microbiol 71:1677–1684CrossRefGoogle Scholar
- Zhao Y, Xia Y, Kana TM, Wu Y, Li X, Yan X (2013) Seasonal variation and controlling factors of anaerobic ammonium oxidation in freshwater river sediments in the Taihu Lake region of China. Chemosphere 93(9):2124-2131Google Scholar
- Zhu Y-G, Su J-Q, Cao Z, Xue K, Quensen J, Guo G-X, Yang Y-F, Zhou J, Chu H-Y, Tiedje JM (2016) A buried Neolithic paddy soil reveals loss of microbial functional diversity after modern rice cultivation. Sci Bull 61(13):1052–1060Google Scholar