Biological conversion pathways of sulfate reduction ammonium oxidation in anammox consortia

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.

Graphical abstract

Keywords

Anammox bacteria / Autotrophic / Biological conversion / Sulfate reducing ammonium oxidation (SRAO)

References

[1] Amend J, Yn K, Rogers L, Shock E, Rieri S, Inguaggiato S (2003). Energetics of chemolithoautotrophy in the hydrothermal system of Volcano Island, southern Italy. Geobiology, 1(1): 37–58

[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] Bi Z, Takekawa M, Park G, Soda S, Zhou J, Qiao S, Ike M (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

[4] Bi Z, Zhang W, Song G, Huang Y (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

[5] Canfield D E, Stewart F J, Thamdrup B, De Brabandere L, Dalsgaard T, Delong E F, Revsbech N P, Ulloa O (2010). A cryptic sulfur cycle in oxygen-minimum-zone waters off the Chilean coast. Science, 330(6009): 1375–1378

[6] Fdz-Polanco F, Fdz-Polanco M, Fernández N, Urueña M A, Garciá P A, Villaverde S (2001a). New process for simultaneous removal of nitrogen and sulphur under anaerobic conditions. Water Research, 35(4): 1111–1114

[7] Fdz-Polanco F, Fdz-Polanco M, Fernández N, Urueña M A, Garciá P A, Villaverde S (2001b). Combining the biological nitrogen and sulfur cycles in anaerobic conditions. Water Science and Technology, 44(8): 77–84

[8] Hao T W, Xiang P Y, Mackey H R, Chi K, Lu H, Chui H K, van Loosdrecht M C, Chen G H (2014). A review of biological sulfate conversions in wastewater treatment. Water Research, 65(1): 1–21

[9] Kartal B, van Niftrik L, Keltjens J T, Op den Camp H J, Jetten M S (2012). Anammox—growth physiology, cell biology, and metabolism. Advances in Microbial Physiology, 60(60): 211–262

[10] Kuypers M M M, Marchant H K, Kartal B (2018). The microbial nitrogen-cycling network. Nature Reviews. Microbiology, 16(5): 263–276

[11] Li W, Zhao Q L, Liu H (2009). Sulfide removal by simultaneous autotrophic and heterotrophic desulfurization-denitrification process. Journal of Hazardous Materials, 162(2-3): 848–853

[12] Liu S, Yang F, Gong Z, Meng F, Chen H, Xue Y, Furukawa K (2008). Application of anaerobic ammonium-oxidizing consortium to achieve completely autotrophic ammonium and sulfate removal. Bioresource Technology, 99(15): 6817–6825

[13] Prachakittikul P, Wantawin C, Noophan P L, Boonapatcharoen N (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

[14] Rikmann E, Zekker I, Tomingas M , Tenno T, Loorits L, Vabamäe P, Mandel A, Raudkivi M, Daija L, Kroon K, Tenno T. (2016). Sulfate-reducing anammox for sulfate and nitrogen containing wastewaters. Desalination and Water Treatment, 57(7): 3132–3141

[15] Rikmann E, Zekker I, Tomingas M, Tenno T, Menert A, Loorits L, Tenno T (2012). Sulfate-reducing anaerobic ammonium oxidation as a potential treatment method for high nitrogen-content wastewater. Biodegradation, 23(4): 509–524

[16] Rikmann E, Zekker I, Tomingas M, Vabamäe P, Kroon K, Saluste A, Tenno T, Menert A, Loorits L, dC Rubin S S, Tenno T (2014). Comparison of sulfate-reducing and conventional Anammox upflow anaerobic sludge blanket reactors. Journal of Bioscience and Bioengineering, 118(4): 426–433

[17] Ruan Y J, Deng Y L, Guo X S, Timmons M B, Lu H F, Han Z Y, Ye Z Y, Shi M M, Zhu S M (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

[18] Sabumon P C (2007). Anaerobic ammonia removal in presence of organic matter: A novel route. Journal of Hazardous Materials, 149(1): 49–59

[19] Sabumon P C (2008). Development of a novel process for anoxic ammonia removal with sulphidogenesis. Process Biochemistry, 43(9): 984–991

[20] Sabumon P C (2009). Effect of potential electron acceptors on anoxic ammonia oxidation in the presence of organic carbon. Journal of Hazardous Materials, 172(1): 280–288

[21] Schrum H N, Spivack A J, Kastner M, D’Hondt S (2009). Sulfate-reducing ammonium oxidation: A thermodynamically feasible metabolic pathway in subseafloor sediment. Geology, 37(10): 939–942

[22] Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor M W, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh B E, Op den Camp H J, van der Drift C, Cirpus I, van de Pas-Schoonen K T, Harhangi H R, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen M A, Mewes H W, Weissenbach J, Jetten M S, Wagner M, Le Paslier D (2006). Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 440(7085): 790–794

[23] Thamdrup B (2012). New pathways and processes in the global nitrogen cycle. Annual Review of Ecology Evolution and Systematics, 43(1): 407–428

[24] van de Graaf A A, de Bruijn P, Robertson L A, Jetten M S M, Kuenen J G (1996). Autotrophic growth of anaerobic ammonium oxidizing microorganisms in a fluidized bed reactor. Microbiology, 142(8): 2187–2196

[25] Wanyan D Q, Huang Y, Bi Z, Liu X, Yao P C, Zhang W J (2017). Conversion pathways of substrates in sulfate-reducing ammonia oxidation system. Environmental Science, 38(8): 3406–3414

[26] Zart D, Bock E (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

[27] Zhang Z, Liu S (2014). Insight into the overconsumption of ammonium by anammox consortia under anaerobic conditions. Journal of Applied Microbiology, 117(6): 1830–1838

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