Effects of Fe(II) on anammox community activity and physiologic response

Highlights

• 0.12 mmol/L Fe(II) enhanced the total anammox activity and bacterial abundance best.

• 0.09 mmol/L Fe(II) led to the best performance on relative anammox activity.

• 0.75 mmol/L Fe(II) had an immediate but recoverable inhibition on anammox activity.

• More genes but not relative level were expressed at higher Fe(II) concentration.

Abstract

Though there are many literatures studying the effects of iron on anammox process, these studies only focus on the reactor performance and/or the microbial community changes, the detailed effects and mechanisms of Fe(II) on anammox bacterial activity and physiology have not been explored. In this study, four Fe(II) concentrations (0.03, 0.09, 0.12 and 0.75 mmol/L) were employed into the enriched anammox culture. The enhancement and inhibition effects of Fe(II) on anammox process and bacterial physiology were investigated. It was discovered that the anammox process and bacterial growth were enhanced by 0.09 and 0.12 mmol/L Fe(II), in which the 0.12 mmol/L Fe(II) had advantage in stimulating the total anammox activity and bacterial abundance, while 0.09 mmol/L Fe(II) enhanced the relative anammox activity better. The anammox activity could be inhibited by 0.75 mmol/L Fe(II) immediately, while the inhibition was recoverable. Both 0.09 and 0.12 mmol/L Fe(II) induced more genes being expressed, while didn’t show a stimulation on the relative expression level of functional genes. And anammox bacteria showed a stress response to detoxify the Fe inhibition once inhibited by 0.75 mmol/L Fe(II). This study provides more information about physiologic response of anammox bacteria to external influence (enhancement and inhibition), and may also instruct the future application of anammox process in treating various sources of wastewater (containing external disturbances such as heavy metals) and/or different treatment strategies (e.g. from side-stream to main-stream).

Graphical abstract

Keywords

Anaerobic ammonium oxidation (Anammox) / Candidatus Kuenenia stuttgartiensis / Ferrous iron / GeoChip

References

[1] Andrews S C (1998). Iron storage in bacteria. Advances in Microbial Physiology, 40: 281–351

[2] Andrews S C, Robinson A K, Rodriguez-Quinones F (2003). Bacterial iron homeostasis. FEMS Microbiology Reviews, 27(2–3): 215–237

[3] APHA (1998). Standard Methods for the Examination of Water and Wastewater, 20th ed. Washington, D.C.: American Public Health Association

[4] Barrangou R (2015). The roles of CRISPR-Cas systems in adaptive immunity and beyond. Current Opinion in Immunology, 32: 36–41

[5] Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero D A, Horvath P (2007). CRISPR provides acquired resistance against viruses in prokaryotes. Science, 315(5819): 1709–1712

[6] Bi Z, Qiao S, Zhou J T, Tang X, Zhang J (2014). Fast start-up of anammox process with appropriate ferrous iron concentration. Bioresource Technology, 170: 506–512

[7] Cua L S, Stein L Y (2011). Effects of nitrite on ammonia-oxidizing activity and gene regulation in three ammonia-oxidizing bacteria. FEMS Microbiology Letters, 319(2): 169–175

[8] Ferousi C, Lindhoud S, Baymann F, Kartal B, Jetten M S, Reimann J (2017). Iron assimilation and utilization in anaerobic ammonium oxidizing bacteria. Current Opinion in Chemical Biology, 37: 129–136

[9] Han P, Huang Y T, Lin J G, Gu J D (2013). A comparison of two 16S rRNA gene-based PCR primer sets in unraveling anammox bacteria from different environmental samples. Applied Microbiology and Biotechnology, 97(24): 10521–10529

[10] He Z L, Gentry T J, Schadt C W, Wu L Y, Liebich J, Chong S C, Huang Z J, Wu W M, Gu B H, Jardine P, Criddle C, Zhou J (2007). GeoChip: A comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME Journal, 1(1): 67–77

[11] Hu B L, Zheng P, Tang C J, Chen J W, Van Der Biezen E, Zhang L, Ni B J, Jetten M S M, Yan J, Yu H Q, Kartal B (2010). Identification and quantification of anammox bacteria in eight nitrogen removal reactors. Water Research, 44(17): 5014–5020

[12] Huang X L, Gao D W, Peng S, Tao Y (2014). Effects of ferrous and manganese ions on anammox process in sequencing batch biofilm reactors. Journal of Environmental Sciences (China), 26(5): 1034–1039

[13] Li X, Hou L, Liu M, Zheng Y, Yin G, Lin X, Cheng L, Li Y, Hu X (2015). Evidence of nitrogen loss from anaerobic ammonium oxidation coupled with ferric iron reduction in an intertidal wetland. Environmental Science & Technology, 49(19): 11560–11568

[14] Liu J F, Sun X B, Yang G C, Mbadinga S M, Gu J D, Mu B Z (2015). Analysis of microbial communities in the oil reservoir subjected to CO₂-flooding by using functional genes as molecular biomarkers for microbial CO₂ sequestration. Frontiers in Microbiology, 6: 236

[15] Liu S T, Horn H (2012). Effects of Fe(II) and Fe(III) on the single-stage deammonification process treating high-strength reject water from sludge dewatering. Bioresource Technology, 114: 12–19

[16] Liu S T, Yang F L, Xue Y, Gong Z, Chen H H, Wang T, Su Z C (2008). Evaluation of oxygen adaptation and identification of functional bacteria composition for anammox consortium in non-woven biological rotating contactor. Bioresource Technology, 99(17): 8273–8279

[17] Liu Y W, Ni B J (2015). Appropriate Fe(II) addition significantly enhances anaerobic ammonium oxidation (anammox) activity through improving the bacterial growth rate. Scientific Reports, 5: 8204

[18] Mak C Y, Lin J G, Chen W H, Ng C A, Bashir M J K (2019). The short- and long-term inhibitory effects of Fe(II) on anaerobic ammonium oxidizing (anammox) process. Water Science and Technology, 79(10): 1860–1867

[19] Op den Camp H J M, Kartal B, Guven D, van Niftrik L A M P, Haaijer S C M, van der Star W R L, van de Pas-Schoonen K T, Cabezas A, Ying Z, Schmid M C, Kuypers M M M, van de Vossenberg J, Harhangi H R, Picioreanu C, van Loosdrecht M C M, Kuenen J G, Strous M, Jetten M S M. (2006). Global impact and application of the anaerobic ammonium-oxidizing (anammox) bacteria. Biochemical Society Transactions, 34(1): 174–178

[20] Oshiki M, Ishii S, Yoshida K, Fujii N, Ishiguro M, Satoh H, Okabe S (2013). Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria. Applied and Environmental Microbiology, 79(13): 4087–4093

[21] Qiao S, Bi Z, Zhou J T, Cheng Y J, Zhang J (2013). Long term effects of divalent ferrous ion on the activity of anammox biomass. Bioresource Technology, 142: 490–497

[22] Ren Y H, Niu J J, Huang W K, Peng D L, Xiao Y H, Zhang X, Liang Y L, Liu X D, Yin H Q (2016). Comparison of microbial taxonomic and functional shift pattern along contamination gradient. BMC Microbiology, 16: 110

[23] Schouten S, Strous M, Kuypers M M M, Rijpstra W I C, Baas M, Schubert C J, Jetten M S M, Damste J S S (2004). Stable carbon isotopic fractionations associated with inorganic carbon fixation by anaerobic ammonium-oxidizing bacteria. Applied and Environmental Microbiology, 70(6): 3785–3788

[24] Shu D T, He Y L, Yue H, Yang S C (2016). Effects of Fe(II) on microbial communities, nitrogen transformation pathways and iron cycling in the anammox process: Kinetics, quantitative molecular mechanism and metagenomic analysis. RSC Advances, 6(72): 68005–68016

[25] Strous M, Jetten M S M (2004). Anaerobic oxidation of methane and ammonium. Annual Review of Microbiology, 58(1): 99–117

[26] 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, Medigue C, Collingro A, Snel B, Dutilh B E, Op Den Camp H J M, 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 M, Wagner M, Le Paslier D (2006). Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 440(7085): 790–794

[27] van Niftrik L, Geerts W J C, Van Donselaar E G, Humbel B M, Webb R I, Fuerst J A, Verkleij A J, Jetten M S M, Strous M (2008a). Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: Cell plan, glycogen storage, and localization of cytochrome c proteins. Journal of Bacteriology, 190(2): 708–717

[28] van Niftrik L, Geerts W J C, Van Donselaar E G, Humbel B M, Yakushevska A, Verkleij A J, Jetten M S M, Strous M (2008b). Combined structural and chemical analysis of the anammoxosome: A membrane-bounded intracytoplasmic compartment in anammox bacteria. Journal of Structural Biology, 161(3): 401–410

[29] van Niftrik L, Jetten M S M (2012). Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiology and Molecular Biology Reviews, 76(3): 585–596

[30] Wang Y Y, Ma X, Zhou S, Lin X M, Ma B, Park H D, Yan Y (2016). Expression of the nirS, hzsA, and hdh genes in response to nitrite shock and recovery in Candidatus Kuenenia stuttgartiensis. Environmental Science & Technology, 50(13): 6940–6947

[31] Yang Y F, Xiao C C, Lu J H, Zhang Y B (2020). Fe(III)/Fe(II) forwarding a new anammox-like process to remove high-concentration ammonium using nitrate as terminal electron acceptor. Water Research, 172: 115528

[32] Zhang X, Chen Z, Zhou Y, Ma Y, Ma C, Li Y, Liang Y, Jia J (2019a). Impacts of the heavy metals Cu(II), Zn(II) and Fe(II) on an anammox system treating synthetic wastewater in low ammonia nitrogen and low temperature: Fe(II) makes a difference. Science of the Total Environment, 648: 798–804

[33] Zhang X, Zhou Y, Zhao S, Zhang R, Peng Z, Zhai H, Zhang H (2018). Effect of Fe(II) in low-nitrogen sewage on the reactor performance and microbial community of an anammox biofilter. Chemosphere, 200: 412–418

[34] Zhang Y, Wang Y Y, Yan Y, Han H C, Wu M (2019b). Characterization of CANON reactor performance and microbial community shifts with elevated COD/N ratios under a continuous aeration mode. Frontiers of Environmental Science & Engineering, 13(1): 7

[35] Zhao J, Zuo J N, Wang X L, Lin J, Yang Y F, Zhou J Z, Chu H J, Li P (2014a). GeoChip-based analysis of microbial community of a combined nitritation-anammox reactor treating anaerobic digestion supernatant. Water Research, 67: 345–354

[36] Zhao R, Zhang H M, Li Y F, Jiang T, Yang F L (2014b). Research of iron reduction and the iron reductase localization of anammox bacteria. Current Microbiology, 69(6): 880–887

Acknowledgements

The authors would like to acknowledge our colleagues, Guangjing Xu and Jun Gu, for supplying the anammox bacterial inoculums, and thank Joy D. Van Nostrand for comments about the manuscript modification. The authors also appreciate the funding support from Start-up Grant (SUG) Nanyang Technological University, Singapore (M4081483.030).

Electronic Supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-020-1299-9 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2020 Higher Education Press