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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2020, Vol. 14 Issue (3) : 38    https://doi.org/10.1007/s11783-019-1217-1
RESEARCH ARTICLE
Biological conversion pathways of sulfate reduction ammonium oxidation in anammox consortia
Zhen Bi1,2, Deqing Wanyan1,2, Xiang Li1,2, Yong Huang1,2()
1. National and Local Joint Engineering Laboratory for Municipal Sewage Resource Utilization Technology, Suzhou 215002, China
2. School of Environment Science and Engineering, Suzhou University of Science and Technology, Suzhou 215002, China
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Abstract

• The SRAO phenomena tended to occur only under certain conditions.

• High amount of biomass and non-anaerobic condition is requirement for SRAO.

• Anammox bacteria cannot oxidize ammonium with sulfate as electron acceptor.

• AOB and AnAOB are mainly responsible for ammonium conversion.

• Heterotrophic sulfate reduction mainly contributed to sulfate conversion.

For over two decades, sulfate reduction with ammonium oxidation (SRAO) had been reported from laboratory experiments. SRAO was considered an autotrophic process mediated by anammox bacteria, in which ammonium as electron donor was oxidized by the electron acceptor sulfate. This process had been attributed to observed transformations of nitrogenous and sulfurous compounds in natural environments. Results obtained differed largely for the conversion mole ratios (ammonium/sulfate), and even the intermediate and final products of sulfate reduction. Thus, the hypothesis of biological conversion pathways of ammonium and sulfate in anammox consortia is implausible. In this study, continuous reactor experiments (with working volume of 3.8L) and batch tests were conducted under normal anaerobic (0.2≤DO<0.5 mg/L) / strict anaerobic (DO<0.2 mg/L) conditions with different biomass proportions to verify the SRAO phenomena and identify possible pathways behind substrate conversion. Key findings were that SRAO occurred only in cases of high amounts of inoculant biomass under normal anaerobic condition, while absent under strict anaerobic conditions for same anammox consortia. Mass balance and stoichiometry were checked based on experimental results and the thermodynamics proposed by previous studies were critically discussed. Thus anammox bacteria do not possess the ability to oxidize ammonium with sulfate as electron acceptor and the assumed SRAO could, in fact, be a combination of aerobic ammonium oxidation, anammox and heterotrophic sulfate reduction processes.

Keywords Anammox bacteria      Autotrophic      Biological conversion      Sulfate reducing ammonium oxidation (SRAO)     
Corresponding Author(s): Yong Huang   
Issue Date: 11 February 2020
 Cite this article:   
Zhen Bi,Deqing Wanyan,Xiang Li, et al. Biological conversion pathways of sulfate reduction ammonium oxidation in anammox consortia[J]. Front. Environ. Sci. Eng., 2020, 14(3): 38.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1217-1
https://academic.hep.com.cn/fese/EN/Y2020/V14/I3/38
Experiment tag Substrates concentration in feed medium Anammox biomass inoculation Filling ratio c) Anaerobic degree d)
NH4+
(mg-N/L)
SO42−
(mg-S/L)
NO3
(mg-N/L)
NO2
(mg-N/L)
Amount (mL) Biomass proportion a) Property b)
CFSTR1 110 0–110 145–0 100 1/30, L F 3.0/3.8 n.a.
CFSTR2 60 90 600 1/5, H D+ P 3.0/3.8 n.a.
CFSTR3 60 90 100 1/30, L D+ P 3.0/3.8 n.a.
Batch1 90 110 100 1/30, L D 3.0/3.8 n.a.
Batch2 90 110 100 1/38, L D 3.8/3.8 s.a.
Batch3 90 160 30 1/21, M D 0.63/0.63 s.a.
Batch4 60 90 600 1/5, H D+ P 3.0/3.8 n.a.
Batch5 60 100 1/30, L D+ P 3.0/3.8 n.a.
Batch6 80 100 50 30 1/21, M D+ P 0.63/0.63 s.a.
Tab.1  Experiments conditions
Fig.1  The procedure scheme of experiments.
Fig.2  The schematic diagram of anaerobic fermentation tank.
Fig.3  Time courses of N-compounds and sulfate concentrations in CFSTR1.
Fig.4  Time courses of N-compounds and sulfate concentrations in CFSTR2.
Fig.5  Time courses of N-compounds and sulfate concentrations in CFSTR3.
Run tag NH4+ (mg-N/L) SO42− (mg-S/L) NO3 (mg-N/L) ORP
(mV)
Initial Final Conversion Initial Final Conversion Initial Final
Batch1 89.38±2.90 72.04±1.50 17.34±3.02 125.00±1.46 125.42±3.07 0.18±1.52 Non-detectable <1 25
Batch2 92.61±1.73 94.14±2.91 1.53±2.52 128.80±2.63 117.28±1.80 11.52±4.38 Non-detectable Non-detectable 490
Batch3 98.94±1.62 98.40±1.72 0.05±0.04 164.56±1.30 135.27±5.60 29.29±6.34 Non-detectable <1 490
Tab.2  Conversion of ammonium and sulfate in Batch1−3
Fig.6  Time courses of N-compounds, sulfate concentration and ORP in Batch4.
Time (d) Ammonium
(mg-N/L)
Nitrite
(mg-N/L)
Nitrate
(mg-N/L)
Nitrogen loss
(mg-N/L)
1 75.67±3.44 0.48±0.08 0.30±0.08 0
2 68.50±2.33 0.16±0.05 0.19±0.05 7.17±1.76
3 51.67±3.11 0±0.02 0.11±0.09 24.00±0.87
4 29.83±3.56 0.25±0.10 0.10±0.11 45.83±2.75
5 15.17±1.89 0.25±0.09 0.09±0.10 60.50±3.12
Tab.3  Ammonium conversion and nitrogen loss in Batch5
Run tag NH4+ (mg-N/L) SO42− (mg-S/L) NO3 (mg-N/L) ORP
(mV)
Initial Final Conversion Initial Final Conversion Initial Final Conversion
Batch6 74.62±4.49 61.68±5.17 12.94±3.58 100.86±1.97 99.78±3.37 0.37±1.92 53.13±3.09 18.71±4.74 34.42±5.49 25
Tab.4  Conversion of ammonium, nitrate and sulfate in Batch6
1 J Amend, K Yn, L Rogers, E Shock, S Rieri, S Inguaggiato (2003). Energetics of chemolithoautotrophy in the hydrothermal system of Volcano Island, southern Italy. Geobiology, 1(1): 37–58
https://doi.org/10.1046/j.1472-4669.2003.00006.x pmid: 19912374
2 American Public Health Association (APHA), American Water Works Association, Water Environment Federation (2005). Standard Methods for the Examination of Water and Wastewater 21st ed., Standard Methods
3 Z Bi, M Takekawa, G Park, S Soda, J Zhou, S Qiao, M Ike (2015). Effects of the C/N ratio and bacterial populations on nitrogen removal in the simultaneous anammox and heterotrophic denitrification process: Mathematic modeling and batch experiments. Chemical Engineering Journal, 280: 606–613
https://doi.org/10.1016/j.cej.2015.06.028
4 Z Bi, W Zhang, G Song, Y Huang (2019). Iron-dependent nitrate reduction by anammox consortia in continuous-flow reactors: A novel prospective scheme for autotrophic nitrogen removal. The Science of the Total Environment, 692: 582–588
https://doi.org/10.1016/j.scitotenv.2019.07.078 pmid: 31539965
5 D E Canfield, F J Stewart, B Thamdrup, L De Brabandere, T Dalsgaard, E F Delong, N P Revsbech, O Ulloa (2010). A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science, 330(6009): 1375–1378
https://doi.org/10.1126/science.1196889 pmid: 21071631
6 F Fdz-Polanco, M Fdz-Polanco, N Fernández, M A Urueña, P A Garciá, S Villaverde (2001a). New process for simultaneous removal of nitrogen and sulphur under anaerobic conditions. Water Research, 35(4): 1111–1114
https://doi.org/10.1016/S0043-1354(00)00474-7 pmid: 11235879
7 F Fdz-Polanco, M Fdz-Polanco, N Fernández, M A Urueña, P A Garciá, S Villaverde (2001b). Combining the biological nitrogen and sulfur cycles in anaerobic conditions. Water Science and Technology, 44(8): 77–84
https://doi.org/10.2166/wst.2001.0469 pmid: 11730140
8 T W Hao, P Y Xiang, H R Mackey, K Chi, H Lu, H K Chui, M C van Loosdrecht, G H Chen (2014). A review of biological sulfate conversions in wastewater treatment. Water Research, 65(1): 1–21
https://doi.org/10.1016/j.watres.2014.06.043 pmid: 25086411
9 B Kartal, L van Niftrik, J T Keltjens, H J Op den Camp, M S Jetten (2012). Anammox—growth physiology, cell biology, and metabolism. Advances in Microbial Physiology, 60(60): 211–262
https://doi.org/10.1016/B978-0-12-398264-3.00003-6 pmid: 22633060
10 M M M Kuypers, H K Marchant, B Kartal (2018). The microbial nitrogen-cycling network. Nature Reviews. Microbiology, 16(5): 263–276
https://doi.org/10.1038/nrmicro.2018.9 pmid: 29398704
11 W Li, Q L Zhao, H Liu (2009). Sulfide removal by simultaneous autotrophic and heterotrophic desulfurization-denitrification process. Journal of Hazardous Materials, 162(2-3): 848–853
https://doi.org/10.1016/j.jhazmat.2008.05.108 pmid: 18599206
12 S Liu, F Yang, Z Gong, F Meng, H Chen, Y Xue, K Furukawa (2008). Application of anaerobic ammonium-oxidizing consortium to achieve completely autotrophic ammonium and sulfate removal. Bioresource Technology, 99(15): 6817–6825
https://doi.org/10.1016/j.biortech.2008.01.054 pmid: 18343660
13 P Prachakittikul, C Wantawin, P L Noophan, N Boonapatcharoen (2016). ANAMMOX-like performances for nitrogen removal from ammonium-sulfate-rich wastewater in an anaerobic sequencing batch reactor. Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 51(3): 220–228
https://doi.org/10.1080/10934529.2015.1094336 pmid: 26634619
14 E Rikmann I , Zekker M , Tomingas T , Tenno L , Loorits P , Vabamäe A , Mandel M , Raudkivi L , Daija K , Kroon T , Tenno . (2016). Sulfate-reducing anammox for sulfate and nitrogen containing wastewaters. Desalination and Water Treatment, 57(7): 3132–3141
https://doi.org/10.1080/19443994.2014.984339
15 E Rikmann, I Zekker, M Tomingas, T Tenno, A Menert, L Loorits, T Tenno (2012). Sulfate-reducing anaerobic ammonium oxidation as a potential treatment method for high nitrogen-content wastewater. Biodegradation, 23(4): 509–524
https://doi.org/10.1007/s10532-011-9529-2 pmid: 22205544
16 E Rikmann, I Zekker, M Tomingas, P Vabamäe, K Kroon, A Saluste, T Tenno, A Menert, L Loorits, S S dC Rubin, T Tenno (2014). Comparison of sulfate-reducing and conventional Anammox upflow anaerobic sludge blanket reactors. Journal of Bioscience and Bioengineering, 118(4): 426–433
https://doi.org/10.1016/j.jbiosc.2014.03.012 pmid: 24863179
17 Y J Ruan, Y L Deng, X S Guo, M B Timmons, H F Lu, Z Y Han, Z Y Ye, M M Shi, S M Zhu (2016). Simultaneous ammonia and nitrate removal in an airlift reactor using poly(butylene succinate) as carbon source and biofilm carrier. Bioresource Technology, 216: 1004–1013
https://doi.org/10.1016/j.biortech.2016.06.056 pmid: 27343453
18 P C Sabumon (2007). Anaerobic ammonia removal in presence of organic matter: A novel route. Journal of Hazardous Materials, 149(1): 49–59
https://doi.org/10.1016/j.jhazmat.2007.03.052 pmid: 17445980
19 P C Sabumon (2008). Development of a novel process for anoxic ammonia removal with sulphidogenesis. Process Biochemistry, 43(9): 984–991
https://doi.org/10.1016/j.procbio.2008.05.004
20 P C Sabumon (2009). Effect of potential electron acceptors on anoxic ammonia oxidation in the presence of organic carbon. Journal of Hazardous Materials, 172(1): 280–288
https://doi.org/10.1016/j.jhazmat.2009.07.006 pmid: 19632034
21 H N Schrum, A J Spivack, M Kastner, S D’Hondt (2009). Sulfate-reducing ammonium oxidation: A thermodynamically feasible metabolic pathway in subseafloor sediment. Geology, 37(10): 939–942
https://doi.org/10.1130/G30238A.1
22 M Strous, E Pelletier, S Mangenot, T Rattei, A Lehner, M W Taylor, M Horn, H Daims, D Bartol-Mavel, P Wincker, V Barbe, N Fonknechten, D Vallenet, B Segurens, C Schenowitz-Truong, C Médigue, A Collingro, B Snel, B E Dutilh, H J Op den Camp, C van der Drift, I Cirpus, K T van de Pas-Schoonen, H R Harhangi, L van Niftrik, M Schmid, J Keltjens, J van de Vossenberg, B Kartal, H Meier, D Frishman, M A Huynen, H W Mewes, J Weissenbach, M S Jetten, M Wagner, D Le Paslier (2006). Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 440(7085): 790–794
https://doi.org/10.1038/nature04647 pmid: 16598256
23 B Thamdrup (2012). New pathways and processes in the global nitrogen cycle. Annual Review of Ecology Evolution and Systematics, 43(1): 407–428
https://doi.org/10.1146/annurev-ecolsys-102710-145048
24 A A van de Graaf, P de Bruijn, L A Robertson, M S M Jetten, J G Kuenen (1996). Autotrophic growth of anaerobic ammonium oxidizing microorganisms in a fluidized bed reactor. Microbiology, 142(8): 2187–2196
25 D Q Wanyan, Y Huang, Z Bi, X Liu, P C Yao, W J Zhang (2017). Conversion pathways of substrates in sulfate-reducing ammonia oxidation system. Environmental Science, 38(8): 3406–3414
pmid: 29964951
26 D Zart, E Bock (1998). High rate of aerobic nitrification and denitrification by Nitrosomonas eutropha grown in a fermentor with complete biomass retention in the presence of gaseous NO2 or NO. Archives of Microbiology, 169(4): 282–286
https://doi.org/10.1007/s002030050573 pmid: 9531628
27 Z Zhang, S Liu (2014). Insight into the overconsumption of ammonium by anammox consortia under anaerobic conditions. Journal of Applied Microbiology, 117(6): 1830–1838
https://doi.org/10.1111/jam.12649 pmid: 25210947
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