Journal of Microbiology and Biotechnology
The Korean Society for Microbiology and Biotechnology publishes the Journal of Microbiology and Biotechnology.

2019 ; Vol.29-12: 1993~2005

AuthorKhulud Alsouleman
Place of dutyDepartment Bioengineering, Leibniz Institute for Agricultural Engineering and Bioeconomy (ATB), Potsdam, Germany,Faculty of Agricultural Sciences, Georg-August-Universität Göttingen, Göttingen, Germany
TitleEffect of Increasing Amounts of Ammonium Nitrogen Induced by Consecutive Mixture of Poultry Manure and Cattle Slurry on the Microbial Community during Thermophilic Anaerobic Digestion
PublicationInfo J. Microbiol. Biotechnol.2019 ; Vol.29-12
AbstractThermophilic 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.
Full-Text
Key_wordAmmonia inhibition, biogas, microbiome, process disturbance
References
  1. 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.
    Pubmed CrossRef
  2. 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.
    CrossRef
  3. 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.
    CrossRef
  4. Abbassi-Guendouz A, Brockmann D, Trably E, Dumas C, Delgenès JP, Steyer JP, et al. 2012. Total solids content drives high solid anaerobic digestion via mass transfer limitation. Bioresour. Technol. 111: 55-61.
    Pubmed CrossRef
  5. Ahring BK. 1993. Perspectives for anaerobic digestion. Adv. Biochem. Eng. Biotechnol. 81: 1-30.
    Pubmed CrossRef
  6. 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.
    Pubmed CrossRef
  7. 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.
    Pubmed CrossRef
  8. Akyol Ç, Turker G, Ince O, Ertekin E, Üstünerc 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.
    Pubmed CrossRef
  9. 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.
    Pubmed CrossRef
  10. 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.
    Pubmed CrossRef
  11. 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.
    Pubmed CrossRef
  12. Hashimoto AG. 1986. Ammonia inhibition of methanogenesis from cattle wastes. Agricultural Wastes. 17: 241-261.
    CrossRef
  13. Koster IW, Lettinga G. 1988. Anaerobic digestion at extreme ammonia concentrations. Biological Wastes. 25:51-59.
    CrossRef
  14. Angelidaki I, Ahring BK. 1993. Thermophilic anaerobic digestion of livestock waste: the effect of ammonia. Appl. Biochem. Biotechnol. 38: 560-564.
    CrossRef
  15. Poggi-Varaldo HM, Rodriguez-Vazquez R, FernandezVillagomez G, Esparza-Garcia F. 1997. Inhibition of mesophilic solid substrate anaerobic digestion by ammonia nitrogen. Appl. Microbiol. Biotechnol. 47: 284-291.
    CrossRef
  16. 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.
    CrossRef
  17. Hansen KH, Angelidaki I, Ahring BK.1998. Anaerobic digestion of swine manure: inhibition by ammonia. Water Res. 32: 5-12.
    CrossRef
  18. Sung S, Liu T. 2003. Ammonia inhibition on thermophilic anaerobic digestion. Chemosphere. 53: 43-52.
    CrossRef
  19. 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.
    CrossRef
  20. 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.
    Pubmed CrossRef
  21. 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.
    Pubmed CrossRef
  22. 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.
    CrossRef
  23. Rademacher A, Nolte C, Schönberg M, Klocke M. 2012. Temperature increases from 55 to 75°C in a two-phase biogas reactor result in fundamental alterations within the bacterial andarchaeal community structure. Appl. Microbiol. Biotechnol. 96: 565-576.
    Pubmed CrossRef
  24. 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.
    Pubmed CrossRef
  25. 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 .
    Pubmed CrossRef
  26. 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.
    CrossRef
  27. Yenigün O, Demirel B. 2013. Ammonia inhibition in anaerobic digestion: a review. Process Biochem. 48: 901-911.
    CrossRef
  28. 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.
    Pubmed CrossRef
  29. 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.
    Pubmed CrossRef
  30. 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.
    Pubmed CrossRef
  31. 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.
    Pubmed CrossRef Pubmed Central
  32. 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.
    CrossRef
  33. 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.
    Pubmed CrossRef
  34. 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.
    Pubmed CrossRef Pubmed Central
  35. TalbotG, Topp E, Palin MF, Massé DI. 2008. Evaluation of molecular methods used for establishing the interactions and functions of microorganisms in anaerobic bioreactors. Water Res. 42: 513-537.
    Pubmed CrossRef
  36. 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.
    Pubmed CrossRef Pubmed Central
  37. Bühligen 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.
    Pubmed CrossRef
  38. 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.
    Pubmed CrossRef Pubmed Central
  39. 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: 1-18.
    Pubmed CrossRef Pubmed Central
  40. VDI (2006) Fermentation of organic materials – Characterisation of the substrate, sampling, collection of material data, fermentation tests. Verein Deutscher Ingenieure.
  41. Schattauer A, Abdoun E, Weiland P, Plöchl M, Heiermann M. 2011. Abundance of trace elements in demonstration biogas plants. Biosyst. Eng. 108: 57-65.
    CrossRef
  42. Schönberg 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.
    CrossRef
  43. Klang J, Theuerl S, Szewzyk U, Huth M, Tölle 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.
    Pubmed CrossRef Pubmed Central
  44. Dufrêne M, Legendre P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67: 345-366.
    CrossRef
  45. McCune B, Mefford MJ. 2011. PC-ORD. Multivariate analysis of ecological data. Version 6.08, Gleneden Beach, Oregon,U.S.A.
  46. Clarke KR.1993. Non-parametric multivariate analyses of changes in community structure. Australian J. Ecol. 18: 117-143.
    CrossRef
  47. 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.
    Pubmed CrossRef
  48. 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.
    Pubmed CrossRef
  49. 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.
    CrossRef
  50. 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.
    Pubmed CrossRef
  51. 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.
    Pubmed CrossRef
  52. 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.
    Pubmed CrossRef Pubmed Central
  53. Pap B, Györkei Á, Boboescu IZ, Nagy IK, Bíró T, Kondorosi É, 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.
    Pubmed CrossRef
  54. 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.
    Pubmed CrossRef
  55. 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.
    CrossRef
  56. Drosg, B. 2013. Process monitoring in biogas plants. In: IEA Bioenergy Task 37 – Energy from Biogas.
  57. 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.
    Pubmed CrossRef
  58. 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.
    Pubmed CrossRef
  59. Zhang W, Werner JJ, Agler MT, Angenent LT. 2014. Substrate type drives variation in reactor microbiomes of anaerobic digesters. Bioresour. Technol. 151: 397-401.
    Pubmed CrossRef
  60. 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.
    Pubmed CrossRef
  61. 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.
    Pubmed CrossRef
  62. Allison SD, Martiny JB. 2008. Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. USA 105: 11512-11519.
    Pubmed CrossRef Pubmed Central
  63. Kovács E, Wirth R, Maróti G, Bagi Z, Rákhely G, Kovács 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.
    Pubmed CrossRef Pubmed Central
  64. Kovács E, Wirth R, Maróti G, Bagi Z, Nagy K, Minárovits J, et al. 2015. Augmented biogas production from protein-rich substrates and associated metagenomic changes. Bioresour. Technol. 178: 254-261.
    Pubmed CrossRef
  65. Westerholm M, Moestedt J, Schnürer A. 2016. Biogas production through syntrophic acetate oxidation and deliberate operating strategies for improved digester performance. Appl. Energy 179: 124-135.
    CrossRef
  66. Dolfing J. 2014. Thermodynamic constrains of SAO. Appl. Environ. Microbiol. 80: 1539-1541.
    Pubmed CrossRef Pubmed Central
  67. 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.
    CrossRef
  68. 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 Management 34: 2080-2089.
    Pubmed CrossRef Pubmed Central
  69. Murto M., Björnsson 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.
    Pubmed CrossRef
  70. Chen Y, Cheng JJ, Creamer KS. 2008. Inhibition of anaerobic digestion process: a review. Bioresour. Technol. 99: 4044-4064.
    Pubmed CrossRef



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