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Differentiation of performance and functional bacteria of anammox processes with different anammox sludge impaired by low temperature

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Abstract

In order to study the differentiation of performance and functional bacteria of anaerobic ammonium oxidation (anammox) processes inoculated with different anammox sludge impaired by low temperature, two upflow anaerobic sludge bed reactors were constructed to treat synthetic nitrogen-contained wastewater. Experimental results showed that anammox sludge exposed to lower room temperature of 0–15 °C for nearly 1 month recovered anammox activity on Day 1 without sludge lysis, and the total nitrogen removal rate (TNRR) gradually increased from 3.23 to 13.41 kg m−3 d−1. Stover–Kincannon model predicted a maximum nitrogen removal potential (Umax) of 177.62 kg m−3 d−1. However, anammox sludge exposed to − 20 °C environment for nearly 30 days experienced three stages of sludge lysis (Days 1–2), sludge lag (Days 3–7) and propagation stage (Days 8–77). Due to the activity loss and FA inhibition, the maximum TNRR of 4.04 kg m−3 d−1 and a predicted Umax of 8.51 kg m−3 d−1 were observed after 77 days’ operation. After long-term operation (291 d), the dominant functional bacteria and genes were changed; even two reactors had similar operation performance. Anammox genus Candidatus Jettenia had the maximum RA values of 16.01% with higher nitrogen removal-related genes nirB/K/S, hdh and hzo in reactor feeding sludge exposed to 0–15 °C, but Candidatus Brocadia was dominant with higher hzs gene in reactor inoculating sludge suffering from − 20 °C environment. This work would be helpful to restart the anammox reactor with seeding sludge after long-term storage of anammox sludge under lower temperature conditions.

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Abbreviations

Anammox:

Anaerobic ammonium oxidation

AnAOB:

Anammox bacteria

AOB:

Ammonia-oxidizing bacteria

DNB:

Denitrifying bacteria

DO:

Dissolved oxygen

FA:

Free ammonia

FNA:

Free nitrous acid

gDNA:

Genomic deoxyribonucleic acid

HRT:

Hydraulic retention time

S-K model:

Stover–Kincannon model

N2 :

Nitrogen gas

NOB:

Nitrite-oxidizing bacteria

R 2 :

Multiple correlation coefficient

RA:

Relative abundance

SAA:

Specific anammox activity

TI:

Trace element concentrated solution I

TII:

Trace element concentrated solution II

TNLR:

Total nitrogen loading rate

TNRR:

Total nitrogen removal rate

UASB:

Upflow anaerobic sludge bed

VSS:

Volatile suspended solids

ΔNH4 +–N:

Removed NH4+–N

ΔNO2 −–N:

Removed NO2−–N

ΔNO3 −–N:

Generated NO3−–N

ΔNO2 −–N/ΔNH4 +–N:

Stoichiometric ratio of removed NO2−–N to removed NH4+–N

ΔNO3 −–N/ΔNH4 +–N:

The stoichiometric ratio of generated NO3−–N to removed NH4+–N

amo :

Ammonia monooxygenase genes

hao :

Hydroxylamine oxidoreductase gene

hdh :

Hydrazine dehydrogenase gene

hox :

Hydroxylamine oxidase gene

hzo :

Hydrazine oxidase gene

HZS:

Hydrazine synthase

hzs :

Hydrazine synthase gene

nar :

Nitrate reductase gene

narA:

Assimilatory nitrate reductase gene

narG:

Membrane-bound nitrate reductase gene

nir :

Nitrite reductases gene

nirB:

Assimilatory nitrite reductases gene

nirK:

Copper-containing nitrite reductases gene

nirS:

Haem-containing nitrite reductases gene

nrf :

Dissimilatory nitrite reductase gene

nxr :

Nitrite oxidoreductase gene

[NH4 +–N]:

Influent and effluent NH4+–N concentration in each reactor, mg L−1

[NO2 −–N]:

Is the influent and effluent NO2−–N concentration, mg L−1

T :

Operation temperature, °C

dS/dt :

Substrates removal rate, kg m−3 d−1

U max :

The maximum substrates removal rate, kg m−3 d−1

K B :

Saturation constant, kg m−3 d−1

Q :

Influent flow rate, m3 d−1

V :

Empty bed volume of the reactor, m3

S 0 :

Influent substrate concentration of anammox reactor, kg m−3

S :

Effluent substrate concentration, kg m−3

References

  • Adams M, Xie JX, Xie JW, Chang YF, Guo ML, Chen CJ, Zhang TC (2020) The effect of carrier addition on Anammox start-up and microbial community: a review. Rev Environ Sci Biotechnol 19:355–368

    Article  CAS  Google Scholar 

  • Aktan CK, Yapsakli K, Mertoglu B (2012) Inhibitory effects of free ammonia on Anammox bacteria. Biodegradation 23:751–762

    Article  CAS  Google Scholar 

  • Ali M, Oshiki M, Okabe S (2014) Simple, rapid and effective preservation and reactivation of anaerobic ammonium oxidizing bacterium “Candidatus Brocadia sinaica”. Water Res 57:215–222

    Article  CAS  Google Scholar 

  • Anthonisen AC, Loehr RC, Prakasam TBS, Srinath EG (1976) Inhibition of nitrification by ammonia and nitrous acid. Water Pollut Control Fed 48(5):835–852

    CAS  Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington

    Google Scholar 

  • Banach-Wisniewska A, Cwiertniewicz-Wojciechowska M, Ziembinska-Buczynska A (2021) Effect of temperature shifts and anammox biomass immobilization on sequencing batch reactor performance and bacterial genes abundance. Int J Environ Sci Technol 18(7):1719–1730

    Article  CAS  Google Scholar 

  • Bilen S, Turan V (2022) Enzymatic analyses in soils. In: Practical handbook on agricultural microbiology. Humana, New York, NY, USA, pp 377–385

  • Chamchoi N, Nitisoravut S (2007) Anammox enrichment from different conventional sludges. Chemosphere 66:2225–2232

    Article  CAS  Google Scholar 

  • Chen H, Jin RC (2017) Summary of the preservation techniques and the evolution of the anammox bacteria characteristics during preservation. Appl Microbiol Biotechnol 101:4349–4362

    Article  CAS  Google Scholar 

  • Ciesielski S, Czerwionka K, Sobotka D, Dulski T, Makinia J (2018) The metagenomic approach to characterization of the microbial community shift during the long-term cultivation of anammox-enriched granular sludge. J Appl Genet 59:109–117

    Article  CAS  Google Scholar 

  • Fernandes LA, Pereira AD, Leal CD, Davenport R, Werner D, Filho CRM, Bressani-Ribeiro T, Chernicharo CAL, Araujo JC (2018) Effect of temperature on microbial diversity and nitrogen removal performance of an anammox reactor treating anaerobically pretreated municipal wastewater. Bioresour Technol 258:208–219

    Article  CAS  Google Scholar 

  • Fernandez I, Dosta J, Fajardo C, Campos JL, Mosquera-Corral A, Mendez R (2012) Short- and long-term effects of ammonium and nitrite on the Anammox process. J Environ Manag 95:S170–S174

    Article  CAS  Google Scholar 

  • Gamoń F, Cema G, Ziembińska-Buczyńska A (2022) The influence of antibiotics on the anammox process—a review. Environ Sci Pollut Res 29:8074–8090

    Article  Google Scholar 

  • Guo JH, Peng YZ, Fan L, Zhang L, Ni BJ, Kartal B, Feng X, Jetten M, Yuan ZG (2016) Metagenomic analysis of anammox communities in three different microbial aggregates. Environ Microbiol 18:2979–2993

    Article  CAS  Google Scholar 

  • He ST, Niu QG, Ma HY (2015) The treatment performance and the bacteria preservation of anammox: a review. Water Air Soil Pollut 226:163

    Article  Google Scholar 

  • Isik M, Sponza T (2005) Substrate removal kinetics in an upflow anaerobic sludge blanket reactor decolorising simulated textile wastewater. Process Biochem 40:1189–1198

    Article  CAS  Google Scholar 

  • Ji YX, Jin RC (2014) Effect of different preservation conditions on the reactivation performance of anammox sludge. Sep Purif Technol 133:32–39

    Article  CAS  Google Scholar 

  • Jin RC, Yang GF, Yu JJ, Zheng P (2012) The inhibition of the anammox process: a review. Chem Eng J 197:67–79

    Article  CAS  Google Scholar 

  • Jung JY, Kang SH, Chung YC, Ahn DH (2007) Factors affecting the activity of anammox bacteria during start up in the continuous culture reactor. Water Sci Technol 55(1–2):459–468

    Article  CAS  Google Scholar 

  • Keren R, Lawrence JE, Zhuang WQ, Jenkins D, Banfield JF, Alvarez-Cohen L, Zhou LJ, Yu K (2020) Increased replication of dissimilatory nitrate-reducing bacteria leads to decreased anammox bioreactor performance. Microbiome 8:7

    Article  CAS  Google Scholar 

  • Khadija K, Mohamed AW, Hamadi K, Andrea F, Alba P, Anuska M, Naceur J (2019) Effects of short- and long-term exposures of humic acid on the anammox activity and microbial community. Environ Sci Pollut Res 26:19012–19024

    Article  Google Scholar 

  • Kindaichi T, Yuri S, Ozaki N, Ohashi A (2012) Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Sci Technol 66(12):2556–2561

    Article  CAS  Google Scholar 

  • Li J, Wang D, Yu DS, Zhang PY (2018) Performance and sludge characteristics of anammox process at moderate and low temperatures. Korean J Chem Eng 35:164–171

    Article  CAS  Google Scholar 

  • Liu YW, Sun J, Peng L, Wang DD, Dai XH, Ni BJ (2016) Assessment of heterotrophic growth supported by soluble microbial products in anammox biofilm using multidimensional modeling. Sci Rep 6:27576

    Article  CAS  Google Scholar 

  • Liu T, Khai Lim Z, Chen H, Hu S, Yuan Z, Guo J (2020) Temperature-tolerated mainstream nitrogen removal by anammox and nitrite/nitrate-dependent anaerobic methane oxidation in a membrane biofilm reactor. Environ Sci Technol 54(5):3012–3021

    Article  CAS  Google Scholar 

  • Liu LJ, Ji M, Wang F, Tian ZK, Yan Z, Wang SY (2021) N-acyl-L-homoserine lactones release and microbial community changes in response to operation temperature in an anammox biofilm reactor. Chemosphere 262:127602

    Article  CAS  Google Scholar 

  • Marcel MMK, Hannah KM, Boran K (2018) The microbial nitrogen-cycling network. Nat Rev Microbiol 16:263–276

    Article  Google Scholar 

  • Ni SQ, Gao BY, Wang CC, Lin JG, Sung S (2011) Fast start-up, performance and microbial community in a pilot-scale anammox reactor seeded with exotic mature granules. Bioresour Technol 102(3):2448–2454

    Article  CAS  Google Scholar 

  • Nobuyuki Y, Ryota M, Hideyuki Y, Tatsuaki H, Hisayoshi I, Takayuki A, Masaaki H, Akihiko T (2019) Startup, performance, and microbial communities of an anammox reactor inoculated with indigenous sludge for the treatment of high-salinity and mesophilic underground brine. Clean Technol Environ 21:1001–1011

    Article  Google Scholar 

  • Nozhevnikova AN, Simankova MV, Litti YuV (2012) Application of the microbial process of anaerobic ammonium oxidation (ANAMMOX) in biotechnological wastewater treatment. Appl Biochem Microbiol 48(8):667–684

    Article  CAS  Google Scholar 

  • Peng YZ, Zhu GB (2006) Biological nitrogen removal with nitrification and denitrification via nitrite pathway. Appl Microbiol Biotechnol 73(1):15–26

    Article  CAS  Google Scholar 

  • Pereira AD, Cabezas A, Etchebehere C, Chernicharo CAL, Araujo JC (2017) Microbial communities in anammox reactors: a review. Environ Technol Rev 6:74–93

    Article  CAS  Google Scholar 

  • Rothrock MJ Jr, Vanotti MB, Szoegi AA, Garcia Gonzalez MC, Fujii T (2011) Long-term preservation of anammox bacteria. Appl Microbiol Biotechnol 92:147–157

    Article  CAS  Google Scholar 

  • Song YX, Ali M, Feng F, Chai XL, Wang S, Wang YY, Tang CJ (2020) Performance of a high-rate anammox reactor under high hydraulic loadings: physicochemical properties, microbial structure and process kinetics. J Cent South Univ 27:1197–1210

    Article  CAS  Google Scholar 

  • Stover EL, Kincannon DF (1982) Rotating biological contactor scale-up and design. In: Proceedings of the 1st international conference on fixed film biological processes. Kings Island, Ohio, USA, pp 1–21

  • Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50:589–596

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Mahmood Q, Chen JW (2009) Start-up and inhibition analysis of the anammox process seeded with anaerobic granular sludge. J Ind Microbiol Biotechnol 36:1093–1100

    Article  CAS  Google Scholar 

  • Tang CJ, Zheng P, Mahmood Q, Chen JW (2010) Effect of substrate concentration on stability of anammox biofilm reactors. J Cent South Univ Technol 17:79–84

    Article  CAS  Google Scholar 

  • Tang CJ, Duan CS, Yu C, Song YX, Chai LY, Xiao RY, Wei ZS, Min XB (2017) Removal of nitrogen from wastewaters by anaerobic ammonium oxidation (ANAMMOX) using granules in upflow reactors. Environ Chem Lett 15(2):311–328

    Article  CAS  Google Scholar 

  • Vlaeminck SE, Geets J, Vervaeren H, Boon N, Verstraete W (2007) Reactivation of aerobic and anaerobic ammonium oxidizers in OLAND biomass after long-term storage. Appl Microbiol Biotechnol 74:1376–1384

    Article  CAS  Google Scholar 

  • Waki M, Tokutomi T, Yokoyama H, Tanaka Y (2007) Nitrogen removal from animal waste treatment water by anammox enrichment. Bioresour Technol 98(14):2775–2780

    Article  CAS  Google Scholar 

  • Wang Y, Bu CN, Kang Q, Ahmad HA, Zhang J, Gao BY, Ni SQ (2017) Autoclaved sludge as the ideal seed to culture anammox bacteria: reactor performance and microbial community diversity. Bioresour Technol 244:391–399

    Article  CAS  Google Scholar 

  • Wang WG, Yan Y, Song CK, Pan ML, Wang YY (2018) The microbial community structure change of an anaerobic ammonia oxidation reactor in response to decreasing temperatures. Environ Sci Pollut Res 25:35330–35341

    Article  CAS  Google Scholar 

  • Wang DP, He Y, Zhang XX (2019) A comprehensive insight into the functional bacteria and genes and their roles in simultaneous denitrification and anammox system at varying substrate loadings. Appl Microbiol Biotechnol 103:1523–1533

    Article  CAS  Google Scholar 

  • Wen XM, Hong YG, Wu JP, Wang Y (2020) Optimization of a method for diversity analysis of anammox bacteria using high-throughput sequencing of 16S rRNA gene amplicon. J Microbiol Methods 178:106066

    Article  CAS  Google Scholar 

  • Wu X, Liu S, Dong G, Hou X (2015) The starvation tolerance of anammox bacteria culture at 35°C. J Biosci Bioeng 120:450–455

    Article  CAS  Google Scholar 

  • Wu P, Chen JJ, Garlapati VK, Zhang XX, Jenario FWV, Li X, Liu WR, Chen CJ, Aminabhavi TM, Zhang XN (2022) Novel insights into anammox-based processes: a critical review. Chem Eng J 444:136534

    Article  CAS  Google Scholar 

  • Xing BS, Guo Q, Jiang XY, Chen QQ, Li P, Ni WM, Jin RC (2016) Influence of preservation temperature on the characteristics of anaerobic ammonium oxidation (anammox) granular sludge. Appl Microbiol Biotechnol 100:4637–4649

    Article  CAS  Google Scholar 

  • Zhang Q, Zhang X, Bai YH, Xia WJ, Ni SK, Wu QY, Fan NS, Huang BC, Jin RC (2020) Exogenous extracellular polymeric substances as protective agents for the preservation of anammox granules. Sci Total Environ 747:141464

    Article  CAS  Google Scholar 

  • Zhao YP, Liu SF, Jiang B, Feng Y, Zhu TT, Tao HC, Tang X, Liu ST (2018) Genome-centered metagenomics analysis reveals the symbiotic organisms possessing ability to cross-feed with anammox bacteria in anammox consortia. Environ Sci Technol 52(19):11285–11296

    Article  CAS  Google Scholar 

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Funding

Funding was provided by National Natural Science Foundation of China (Grant Nos. 51808498, 52070169), Natural Science Foundation of Zhejiang Province of China (Grant Nos. Y23E080032, LQ17E090002) and Zhejiang Provincial Ten Thousand Plan for Young Top Talents (No. 2019R51005).

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Authors and Affiliations

  1. Department of Environmental Science and Engineering, Zhejiang Ocean University, No.1 Haida South Road, Zhoushan, 316022, People’s Republic of China

    G. Yang, Y. Li, Y. Liu, Y. Zhao, Y. Fang, J. Chen & D. Chen

  2. Zhejiang Provincial Key Laboratory of Petrochemical Environmental Pollution Control, Zhoushan, 316022, People’s Republic of China

    G. Yang, J. Chen & D. Chen

  3. Department of Environmental Sciences, Hangzhou Normal University, Hangzhou, 310036, People’s Republic of China

    R. Jin

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  1. G. Yang
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Correspondence to D. Chen.

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Yang, G., Li, Y., Liu, Y. et al. Differentiation of performance and functional bacteria of anammox processes with different anammox sludge impaired by low temperature. Int. J. Environ. Sci. Technol. 20, 12053–12068 (2023). https://doi.org/10.1007/s13762-022-04747-y

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