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http://dx.doi.org/10.4014/jmb.1909.09023

Effect of Increasing Amounts of Ammonium Nitrogen Induced by Consecutive Mixture of Poultry Manure and Cattle Slurry on the Microbial Community during Thermophilic Anaerobic Digestion  

Alsouleman, Khulud (Department Bioengineering, Leibniz Institute for Agricultural Engineering and Bioeconomy (ATB))
Publication Information
Journal of Microbiology and Biotechnology / v.29, no.12, 2019 , pp. 1993-2005 More about this Journal
Abstract
Thermophilic anaerobic digestion (TAD) is characterized by higher biogas production rates as a result of assumedly faster microbial metabolic conversion rates compared to mesophilic AD. It was hypothesized that the thermophilic microbiome with its lower diversity than the mesophilic one is more susceptible to disturbances introduced by alterations in the operating factors, as an example, the supply of nitrogen-rich feedstock such as poultry manure (PM). Laboratory scaled TAD experiments using cattle slurry and increasing amounts of PM were carried out to investigate the (in-) stability of the process performance caused by the accumulation of ammonium and ammonia with special emphasis on the microbial community structure and its dynamic variation. The results revealed that the moderate PM addition, i.e., 25% (vol/vol based on volatile substances) PM, resulted in a reorganization of the microbial community structure which was still working sufficiently. With 50% PM application, the microbial community was further stepwise re-organized and was able to compensate for the high cytotoxic ammonia contents only for a short time resulting in consequent process disturbance and final process failure. This study demonstrated the ability of the acclimated thermophilic microbial community to tolerate a certain amount of nitrogen-rich substrate.
Keywords
Ammonia inhibition; microbiome; process disturbance; biogas;
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1 Ji Y, Angel R, Klose M, Claus P, Marotta H, Pinho L, et al. 2016. Structure and function of methanogenicmicrobial communities in sediments of Amazonian lakes with different water types. Environ. Microbiol. 18: 5082-5100.   DOI
2 Van Goethem MW, Makhalanyane TP, Valverde A, Cary SC, Cowan DA. 2016. Characterization of bacterial communities in lithobionts and soil niches from Victoria Valley, Antarctica. FEMS Microbiol. Ecol. 92: fiw051.   DOI
3 VDI. 2006. Fermentation of organic materials - Characterisation of the substrate, sampling, collection of material data, fermentation tests. Verein Deutscher Ingenieure.
4 Schattauer A, Abdoun E, Weiland P, Plochl M, Heiermann M. 2011. Abundance of trace elements in demonstration biogas plants. Biosyst. Eng. 108: 57-65.   DOI
5 Schonberg M, Linke B. 2012. The influence of the temperature regime on the formation of methane in a twophase anaerobic digestion process. Eng. Life Sci. 12: 279-286.   DOI
6 Klang J, Theuerl S, Szewzyk U, Huth M, Tolle R, Klocke M. 2015. Dynamic variation of the microbial community structure during the long- time mono- fermentation of maize and sugar beet silage. Microb. Biotechnol. 8: 764-775.   DOI
7 Dufrêne M, Legendre P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67: 345-366.   DOI
8 McCune B, Mefford MJ. 2011. PC-ORD. Multivariate analysis of ecological data. Version 6.08, Gleneden Beach, Oregon, U.S.A.
9 Clarke KR.1993. Non-parametric multivariate analyses of changes in community structure. Australian J. Ecol. 18: 117-143.   DOI
10 Theuerl S, Kohrs F, Benndorf D, Maus I, Wibberg D, Schlüter A, et al. 2015. Community shifts in a well-operating agricultural biogas plant: how process variations are handled by the microbiome, Appl. Microbiol. Biotechnol. 99: 7791-7803.   DOI
11 Carballa M, Smits M, Etchebehere C, Boon N, Verstraete W. 2011. Correlations between molecular and operational parameters in continuous lab-scale anaerobic reactors. Appl. Microbiol. Biotechnol. 89: 303-314.   DOI
12 Verstraete W, Wittebolle L, Heylen K, Vanparys B, de Vos P, van de Wiele T, et al. 2007. Microbial resource management: the road to go for environmental biotechnology. Eng. Life Sci. 7: 117-126.   DOI
13 Abbassi-Guendouz A, Brockmann D, Trably E, Dumas C, Delgenes JP, Steyer JP, et al. 2012. Total solids content drives high solid anaerobic digestion via mass transfer limitation. Bioresour. Technol. 111: 55-61.   DOI
14 Barret M, Gagnon N, Morissette B, Kalmokoff ML, Topp E, Brooks SPJ, et al. 2015. Phylogenetic identification of methanogens assimilating acetate-derived carbon in dairy and swine manures. Syst. Appl. Microbiol. 38: 56-66.   DOI
15 Börjesson P, Berglund M. 2007. Environmental systems analysis of biogas systems - Part II: Environmental impact of replacing various reference systems. Biomass Bioenergy 31: 326-344.   DOI
16 Arthurson V. 2009. Closing the global energy and nutrient cycles through application of biogas residues to agricultural land - potential benefits and drawbacks. Energies 2: 226-242.   DOI
17 Hansen KH, Angelidaki I, Ahring BK.1998. Anaerobic digestion of swine manure: inhibition by ammonia. Water Res. 32: 5-12.   DOI
18 Angelidaki I, Ahring BK. 1993. Thermophilic anaerobic digestion of livestock waste: the effect of ammonia. Appl. Biochem. Biotechnol. 38: 560-564.
19 Poggi-Varaldo HM, Rodriguez-Vazquez R, Fernandez-Villagomez G, Esparza-Garcia F. 1997. Inhibition of mesophilic solid substrate anaerobic digestion by ammonia nitrogen. Appl. Microbiol. Biotechnol. 47: 284-291.   DOI
20 Gallert C, Winter J. 1997. Mesophilic and thermophilic anaerobic digestion of source-sorted organic wastes: effect of ammonia on glucose degradation and methane production. Appl. Microbiol. Biotechnol. 48: 405-410.   DOI
21 Ziganshina1 EE, Belostotskiy DE, Shushlyaev RV, Miluykov VA, Vankov PY, Ziganshin AM. 2014. Microbial community diversity in anaerobic reactors digesting turkey, chicken, and swine wastes. J. Microbiol. Biotechnol. 24: 1464-1472.   DOI
22 Niu Q, Takemura Y, Kubota K, Li Y Y. 2015 . Comparing mesophilic and thermophilic anaerobic digestion of chicken manure: microbial community dynamics and process resilience. Waste Manag. 43: 114-122.   DOI
23 De Vrieze J, Saunders AM, He Y, Fang J, Nielsen PH, Verstraete W, et al. 2015. Ammonia and temperature determine potential clustering in the anaerobic digestion microbiome. Water Res. 75: 312-323.   DOI
24 Campanaro S, Treu L, Kougias PG, de Francisci D, Valle G, Angelidaki I. 2016. Metagenomic analysis and functional characterization of the biogas microbiome using high throughput shotgun sequencing and a novel binning strategy. Biotechnol. Biofuels. 9: 26.   DOI
25 Lu X, Rao S, Shen Z, Lee PKH. 2013. Substrate induced emergence of different active bacterial and archaeal assemblages during biomethane production. Bioresour. Technol. 148: 517-524.   DOI
26 Zhang W, Werner JJ, Agler MT, Angenent LT. 2014. Substrate type drives variation in reactor microbiomes of anaerobic digesters. Bioresour. Technol. 151: 397-401.   DOI
27 Hao L, Lü F, Mazéas L, Quémnér ED, Madigou C, Guenne A, et al. 2015. Stable isotope probing of acetate fed anaerobic batch incubations shows a partial resistance of acetoclastic methanogenesis catalyzed by Methanosarcina to sudden increase of ammonia level. Water Res. 69: 90-99.   DOI
28 Sung S, Liu T. 2003. Ammonia inhibition on thermophilic anaerobic digestion. Chemosphere 53: 43-52.   DOI
29 Nakakubo R, Moller HB, Nielsen AM, Matsuda J. 2008. Ammonia inhibition ofmethanogenesis and identification of process indicators during anaerobic digestion. Environ. Eng. Sci. 25: 1487-1496.   DOI
30 Alsouleman K, Linke B, Klang J, Klocke M, Krakat N, Theuerl S. 2016. Reorganisation of a mesophilic biogas microbiome as response to a stepwise increase of ammonium nitrogen induced by poultry manure supply. Bioresour. Technol. 208: 200-204.   DOI
31 Fotidis I, Karakashev D, Angelidaki I. 2014. The dominant acetate degradation pathway/methanogenic composition in full-scale anaerobic digesters operating under different ammonia levels. Int. J. Environ. SciTe. 11: 2087-2094.   DOI
32 Drosg, B. 2013. Process monitoring in biogas plants. In: IEA Bioenergy Task 37 - Energy from Biogas.
33 Pap B, Gyorkei A, Boboescu IZ, Nagy IK, Biro T, Kondorosi E, et al. 2015. Temperaturedependent transformation of biogasproducing microbial communities points to the increased importance of hydrogenotrophic methanogenesis under thermophilic operation. Bioresour. Technol. 177: 375-380.   DOI
34 Lv Z, Hu M, Harms H, Richnow HH, Liebetrau J, Nikolausz M. 2014. Stable isotope composition of biogas allows early warning of complete process failure as a result of ammonia inhibition in anaerobic digesters. Bioresour. Technol. 167: 251-259.   DOI
35 Wang Y, Zhang Y, Wang J, Meng L. 2009. Effects of volatile fatty acid concentrations on methane yield and methanogenic bacteria. Biomass Bioenergy 33: 848-853.   DOI
36 De Vrieze J, Christiaens MER, Walraedt D, Devooght A, Ijaz UZ, Boon N. 2017. Microbial community redundancy in anaerobic digestion drives process recovery after salinity exposure. Water Res. 111: 109-117.   DOI
37 Kovács E, Wirth R, Maroti G, Bagi Z, Nagy K, Minarovits J, et al. 2015. Augmented biogas production from protein-rich substrates and associated metagenomic changes. Bioresour. Technol. 178: 254-261.   DOI
38 Louca S, Polz MF, Mazel F, Albright MBN, Huber JA, O'Connor MI, et al. 2018. Function and functional redundancy in microbial systems. Nat. Ecol. Evol. 2:936-943.   DOI
39 Allison SD, Martiny JB. 2008. Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. USA 105: 11512-11519.   DOI
40 Kovacs E, Wirth R, Maroti G, Bagi Z, Rakhely G, Kovacs KL. 2013. Biogas production from protein-rich biomass: fedbatch anaerobic fermentation of casein and of pig blood and associated changes in microbial community composition, PLoS One 8: e77265.   DOI
41 Westerholm M, Moestedt J, Schnurer A. 2016. Biogas production through syntrophic acetate oxidation and deliberate operating strategies for improved digester performance. Appl. Energy 179: 124-135.   DOI
42 Dolfing J. 2014. Thermodynamic constrains of SAO. Appl. Environ. Microbiol. 80: 1539-1541.   DOI
43 Chen Y, Cheng JJ, Creamer KS. 2008. Inhibition of anaerobic digestion process: a review. Bioresour. Technol. 99: 4044-4064.   DOI
44 Amani T, Nosrati M, Sreekrishnan T R. 2010. Anaerobic digestion from the viewpoint of microbiological, chemical, and operational aspects - a review. Environ. Rev. 18: 255-278.   DOI
45 Whittle IHF, Walter A, Ebner C, Insam H. 2014. Investigation into the effect of high concentrations of volatile fatty acids in anaerobic digestion on methanogenic communities. Waste Manag. 34: 2080-2089.   DOI
46 Murto M, Bjornsson L, Mattiasson B. 2004. Impact of food industrial waste on anaerobic co-digestion of sewage sludge and pig manure. J. Environ. Manage. 70: 101-107.   DOI
47 Akyol C, Turker G, Ince O, Ertekin E, Ustunerc O, Incea B. 2016. Performance and microbial community variations in thermophilic anaerobic digesters treating OTC medicated cow manure under different operational conditions. Bioresour. Technol. 205: 191-198.   DOI
48 Ahring BK. 1993. Perspectives for anaerobic digestion. Adv. Biochem. Eng. Biotechnol. 81: 1-30.
49 Shi J, Wang Z, Stiverson JA, Yu Z, Li Y. 2013. Reactor performance and microbial community dynamics during solid-state anaerobic digestion of corn stover at mesophilic and thermophilic conditions. Bioresour. Technol. 136: 574-581.   DOI
50 Wilson CA, Murthy SM, Fang Y, Novak JT. 2008. The effect of temperature on the performance and stability of thermophilic anaerobic digestion. Water Sci. Technol. 57: 297-304.   DOI
51 Guo X, Wang C, Sun F, Zhu W, Wu W. 2014. A comparison of microbial characteristics between the thermophilic and mesophilic anaerobic digesters exposed to elevated food waste loadings. Bioresour. Technol. 152: 420-428.   DOI
52 Hori T, Haruta S, Sasaki D, Hanajima D, Ueno Y, Ogata A, et al. 2015. Reorganization of the bacterial and archaeal populations associated with organic loading conditions in a thermophilic anaerobic digester. J. Biosci. Bioeng. 19: 337-344.
53 Niu QG, Qiao W, Qiang H, Li YY. 2013. Microbial community shifts and biogas conversion computation during steady, inhibited and recovered stages of thermophilic methane fermentation on chicken manure with a wide variation of ammonia. Bioresour. Technol. 146: 223-233.   DOI
54 Hashimoto AG. 1986. Ammonia inhibition of methanogenesis from cattle wastes. Agricultural Wastes. 17: 241-261.   DOI
55 Koster IW, Lettinga G. 1988. Anaerobic digestion at extreme ammonia concentrations. Biological Wastes. 25:51-59.   DOI
56 TalbotG, Topp E, Palin MF, Masse DI. 2008. Evaluation of molecular methods used for establishing the interactions and functions of microorganisms in anaerobic bioreactors. Water Res. 42: 513-537.   DOI
57 Weise L, Ulrich A, Moreano M, Gessler A, Kayler ZE, Steger K, et al. 2016. Water level changesaffect carbon turnover and microbial community composition in lake sediments. FEMS Microbiol. Ecol. 92: fiw035.   DOI
58 Cabezas A, de Araujo JC, Callejas C, Gales, A. Hamelin J, Marone A, et al. 2015. How to use molecular biology tools for the study of the anaerobic digestion process? Rev. Environ. Sci. Bio-Technol. 14: 555-593.   DOI
59 Van Dorst J, Bissett A, Palmer AS, Brown M, Snape I, Stark JS, et al. 2014. Community fingerprinting in a sequencing world. FEMS Microbiol. Ecol. 89: 316-330.   DOI
60 Sboner A, Mu XJ, Greenbaum D, Auerbach RK, Gerstein MB. 2011. The real cost of sequencing: higher than you think! Genome Biol. 12(8): 125.   DOI
61 De Vrieze J, Ijaz UZ, Saunders AM, Theuerl S. 2018. Terminal restriction fragment length polymorphism is an "old school" reliable technique for swift microbial community screening in anaerobic digestion. Sci. Rep. 8: 16818.   DOI
62 Buhligen F, Lucas R, Nikolausz M, Kleinsteuber SA.2016. T-RFLP database for the rapid profiling of methanogenic communities in anaerobic digesters. Anaerobe. 39: 114-116.   DOI
63 Prakash O, Pandey PK, Kulkarni GJ, Mahale KN, Shouche YS. 2014. Technicalities and glitches of terminal restriction fragment length polymorphism (T-RFLP). Indian J. Microbiol. 54: 255-261.   DOI
64 Weissbrodt DG, Shani N, Sinclair L, Lefebvre G,Rossi P, Maillard J, et al. 2012. PyroTRF-ID: a novel bioinformatics methodology for the affiliation of terminalrestriction fragments using 16S rRNA gene pyrosequencing data. BMC Microbiol. 12: 1306.
65 Niu Q, Kubota K, Qiao W, Jing Z, Zhang Y, Yu-You L. 2014. Effect of ammonia inhibition on microbial community dynamic and process functional resilience in mesophilic methane fermentation of chicken manure. J. Chem. Technol. Biotechnol. 90: 2161-2169.
66 Rademacher A, Nolte C, Schonberg M, Klocke M. 2012. Temperature increases from 55 to 75$^{\circ}C$ in a two-phase biogas reactor result in fundamental alterations within the bacterial andarchaeal community structure. Appl. Microbiol. Biotechnol. 96: 565-576.   DOI
67 Yabu H, Sakai C, Fujiwara T, Nishio N, Nakashimada Y. 2011. Thermophilic two-stage dryanaerobic digestion of model garbage with ammonia stripping. J. Biosci. Bioeng. 111: 312-319.   DOI
68 Weiss A, Jérôme V, Freitag R, Mayer HK. 2008. Diversity of the resident microbiota in a thermophilic municipal biogas plant. Appl. Microbiol. Biotechnol. 81: 163-173 .   DOI
69 Yenigün O, Demirel B. 2013. Ammonia inhibition in anaerobic digestion: a review. Process Biochem. 48: 901-911.   DOI
70 Hill R, Saetnan ER, Scullion J, Gwynn-Jones D, Ostle N, Edwardset A.2016. Temporal and spatial influences incur reconfiguration of Arctic heathland soil bacterial community structure. Environ. Microbiol. 18: 1942-1953.   DOI