Abstract
The aim of this study was to investigate how the microbial community structure adapts during the start-up phase and how the 13C fractionation of biogas reflects the microbial population dynamics in two parallel swine manure–fed anaerobic digesters. Two swine manure–fed reactors for the start-up of continuously stirred tank reactors at mesophilic condition were evaluated. Changes in community structure were monitored using 16S rRNA high-throughput sequencing to measure the abundance of fermenting bacteria and methanogens. Digesters with relatively stable Methanosarcinaceae started up successfully and contained high gas production and low levels of propionate. In contrast, the digester that experienced a difficult start-up period had reduced Methanosarcinaceae along with accumulated propionate and low gas production. Specific gas production, specific methane production, and 13C fractionation of biogas were influenced significantly by Methanosarcinaceae, Methanobacteriaceae, and Clostridiaceae, indicating that the 13C fractionation of biogas had significant potential to reflect microbial population changes and digester performance during the start-up period.
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References
Amha YM, Anwar MZ, Brower A, Jacobsen CS, Stadler LB, Webster TM, Smith AL (2018) Inhibition of anaerobic digestion processes: applications of molecular tools. Bioresour Technol 247:999–1014. https://doi.org/10.1016/j.biortech.2017.08.210
Angelidaki I, Chen XX, Cui JB, Kaparaju P, Ellegaard L (2006) Thermophilic anaerobic digestion of source-sorted organic fraction of household municipal solid waste: start-up procedure for continuously stirred tank reactor. Water Res 40:2621–2628. https://doi.org/10.1016/j.watres.2006.05.015
Ariesyady HD, Ito T, Okabe S (2007) Functional bacterial and archaeal community structures of major trophic groups in a full-scale anaerobic sludge digester. Water Res 41:1554–1568. https://doi.org/10.1016/j.watres.2006.12.036
Bolzonella D, Battistoni P, Mata-Alvarez J, Cecchi F (2003a) Anaerobic digestion of organic solid wastes: process behaviour in transient conditions. Water Sci Technol 48:1–8
Bolzonella D, Innocenti L, Pavan P, Traverso P, Cecchi F (2003b) Semi-dry thermophilic anaerobic digestion of the organic fraction of municipal solid waste: focusing on the start-up phase. Bioresour Technol 86:123–129. https://doi.org/10.1016/S0960-8524(02)00161-X
Botsch KC, Conrad R (2011) Fractionation of stable carbon isotopes during anaerobic production and degradation of propionate in defined microbial cultures. Org Geochem 42:289–295. https://doi.org/10.1016/j.orggeochem.2011.01.005
Brambilla M, Araldi F, Marchesi M, Bertazzoni B, Zagni M, Navarotto P (2012) Monitoring of the startup phase of one continuous anaerobic digester at pilot scale level. Biomass Bioenergy 36:439–446. https://doi.org/10.1016/j.biombioe.2011.11.009
Castellari M, Versari A, Spinabelli U, Galassi S, Amati A (2000) An improved HPLC method for the analysis of organic acids, carbohydrates, and alcohols in grape musts and wines. J Liq Chromatog R T 23:2047–2056. https://doi.org/10.1081/JLC-100100472
Chackhiani M, Dabert P, Abzianidze T, Partskhaladze G, Tsiklauri L, Dudauri T, Godon JJ (2004) 16S rDNA characterisation of bacterial and archaeal communities during start-up of anaerobic thermophilic digestion of cattle manure. Bioresour Technol 93:227–232. https://doi.org/10.1016/j.biortech.2003.11.005
Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99:4044–4064. https://doi.org/10.1016/j.biortech.2007.01.057
De Vrieze J, De Waele M, Boeckx P, Boon N (2018) Isotope fractionation in biogas allows direct microbial community stability monitoring in anaerobic digestion. Environ Sci Technol 52:6704–6713. https://doi.org/10.1021/acs.est.8b00723
del Pozo R, Diez V, Salazar G (2002) Start-up of a pilot-scale anaerobic fixed film reactor at low temperature treating slaughterhouse wastewater. Water Sci Technol 46:215–221
Doloman A, Soboh Y, Walters AJ, Sims RC, Miller CD (2017) Qualitative analysis of microbial dynamics during anaerobic digestion of microalgal biomass in a UASB reactor. Int J Microbiol 2017:5291283–5291212. https://doi.org/10.1155/2017/5291283
Feisthauer S, Siegert M, Seidel M, Richnow HH, Zengler K, Gründger F, Krüger M (2010) Isotopic fingerprinting of methane and CO2 formation from aliphatic and aromatic hydrocarbons. Org Geochem 41:482–490. https://doi.org/10.1016/j.orggeochem.2010.01.003
Feng L, Casas ME, Ottosen LDM, Moller HB, Bester K (2017) Removal of antibiotics during the anaerobic digestion of pig manure. Sci Total Environ 603:219–225. https://doi.org/10.1016/j.scitotenv.2017.05.280
Friendly M (2002) Corrgrams: exploratory displays for correlation matrices. Am Stat 56:316–324
Galand PE, Yrjälä K, Conrad R (2010) Stable carbon isotope fractionation during methanogenesis in three boreal peatland ecosystems. Biogeosci Discuss 7:5497–5515
Ganesh R, Torrijos M, Sousbie P, Lugardon A, Steyer JP, Delgenes JP (2014) Single-phase and two-phase anaerobic digestion of fruit and vegetable waste: comparison of start-up, reactor stability and process performance. Waste Manag 34:875–885. https://doi.org/10.1016/j.wasman.2014.02.023
Gao SM, Zhao MX, Chen Y, Yu MJ, Ruan WQ (2015) Tolerance response to in situ ammonia stress in a pilot-scale anaerobic digestion reactor for alleviating ammonia inhibition. Bioresour Technol 198:372–379. https://doi.org/10.1016/j.biortech.2015.09.044
Gonzalez-Gil L, Mauricio-Iglesias M, Serrano D, Lema JM, Carballa M (2018) Role of methanogenesis on the biotransformation of organic micropollutants during anaerobic digestion. Sci Total Environ 622:459–466. https://doi.org/10.1016/j.scitotenv.2017.12.004
Griffin ME, McMahon KD, Mackie RI, Raskin L (1998) Methanogenic population dynamics during start-up of anaerobic digesters treating municipal solid waste and biosolids. Biotechnol Bioeng 57:342–355
Hansen KH, Angelidaki I, Ahring BK (1998) Anaerobic digestion of swine manure: inhibition by ammonia. Water Res 32:5–12. https://doi.org/10.1016/S0043-1354(97)00201-7
Hansen KH, Angelidaki I, Ahring BK (1999) Improving thermophilic anaerobic digestion of swine manure. Water Res 33:1805–1810. https://doi.org/10.1016/S0043-1354(98)00410-2
Keppler F, Laukenmann S, Rinne J, Heuwinkel H, Greule M, Whiticar M, Lelieveld J (2010) Measurements of C-13/C-12 methane from anaerobic digesters: comparison of optical spectrometry with continuous-flow isotope ratio mass spectrometry. Environ Sci Technol 44:5067–5073
Lepisto SS, Rintala JA (1995) Thermophilic Anaerobic-Digestion of the Organic Fraction of Municipal Solid-Waste - Start-up with Digested Material from a Mesophilic Process. Environ Technol 16:157–164. https://doi.org/10.1080/09593331608616256
Li YB, Park SY, Zhu JY (2011) Solid-state anaerobic digestion for methane production from organic waste. Renew Sust Energ Rev 15:821–826. https://doi.org/10.1016/j.rser.2010.07.042
Lian S, Nikolausz M, Nijenhuis I, Leite AF, Richnow HH (2018) Biotransformation and inhibition effects of hexachlorocyclohexanes during biogas production from contaminated biomass characterized by isotope fractionation concepts. Bioresour Technol 250:683–690
Lv Z, Hu M, Harms H, Richnow HH, Liebetrau J, Nikolausz M (2014a) 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. https://doi.org/10.1016/j.biortech.2014.06.029
Lv Z, Leite AF, Harms H, Richnow HH, Liebetrau J, Nikolausz M (2014b) Influences of the substrate feeding regime on methanogenic activity in biogas reactors approached by molecular and stable isotope methods. Anaerobe 29:91–99. https://doi.org/10.1016/j.anaerobe.2013.11.005
Lv Z, Leite AF, Harms H, Glaser K, Liebetrau J, Kleinsteuber S, Nikolausz M (2018) Microbial community shifts in biogas reactors upon complete or partial ammonia inhibition. Appl Microbiol Biotechnol 103:519–533. https://doi.org/10.1007/s00253-018-9444-0
Lv Z, Chen Z, Chen X, Liang J, Jiang J, Loake GJ (2019) Effects of various feedstocks on isotope fractionation of biogas and microbial community structure during anaerobic digestion. Waste Manag 84:211–219. https://doi.org/10.1016/j.wasman.2018.11.043
McMahon KD, Zheng D, Stams AJ, Mackie RI, Raskin L (2004) Microbial population dynamics during start-up and overload conditions of anaerobic digesters treating municipal solid waste and sewage sludge. Biotechnol Bioeng 87:823–834. https://doi.org/10.1002/bit.20192
Micolucci F, Gottardo M, Cavinato C, Pavan P, Bolzonella D (2016) Mesophilic and thermophilic anaerobic digestion of the liquid fraction of pressed biowaste for high energy yields recovery. Waste Manag 48:227–235. https://doi.org/10.1016/j.wasman.2015.09.031
Mosbaek F, Kjeldal H, Mulat DG, Albertsen M, Ward AJ, Feilberg A, Nielsen JL (2016) Identification of syntrophic acetate-oxidizing bacteria in anaerobic digesters by combined protein-based stable isotope probing and metagenomics. ISME J 10:2405–2418. https://doi.org/10.1038/ismej.2016.39
Narihiro T, Sekiguchi Y (2007) Microbial communities in anaerobic digestion processes for waste and wastewater treatment: a microbiological update. Curr Opin Biotechnol 18:273–278. https://doi.org/10.1016/j.copbio.2007.04.003
Nelson MC, Morrison M, Yu ZT (2011) A meta-analysis of the microbial diversity observed in anaerobic digesters. Bioresour Technol 102:3730–3739. https://doi.org/10.1016/j.biortech.2010.11.119
Nikolausz M, Walter RFH, Sträuber H, Liebetrau J, Schmidt T, Kleinsteuber S, Bratfisch F, Günther U, Richnow HH (2013) Evaluation of stable isotope fingerprinting techniques for the assessment of the predominant methanogenic pathways in anaerobic digesters. Appl Microbiol Biotechnol 97:2251–2262. https://doi.org/10.1007/s00253-012-4657-0
Ros M, Oliveira JD, Murcia MDP, Bustamante MA, Moral R, Coll MD, Santisima-Trinidad ABL, Pascual JA (2017) Mesophilic anaerobic digestion of pig slurry and fruit and vegetable waste: dissection of the microbial community structure. J Clean Prod 156:757–765. https://doi.org/10.1016/j.jclepro.2017.04.110
Schuchmann K, Müller V (2014) Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol 12:809–821. https://doi.org/10.1038/nrmicro3365
Strauber H, Lucas R, Kleinsteuber S (2016) Metabolic and microbial community dynamics during the anaerobic digestion of maize silage in a two-phase process. Appl Microbiol Biotechnol 100:479–491. https://doi.org/10.1007/s00253-015-6996-0
Sui QW, Meng XS, Wang R, Zhang JY, Yu DW, Chen MX, Wang YW, Wei YS (2018) Effects of endogenous inhibitors on the evolution of antibiotic resistance genes during high solid anaerobic digestion of swine manure. Bioresour Technol 270:328–336. https://doi.org/10.1016/j.biortech.2018.09.043
van der Wielen PWJJ, Rovers GMLL, Scheepens JMA, Biesterveld S (2002) Clostridium lactatifermentans sp nov., a lactate-fermenting anaerobe isolated from the caeca of a chicken. Int J Syst Evol Microbiol 52:921–925. https://doi.org/10.1099/00207713-52-3-921
Vanwonterghem I, Jensen PD, Dennis PG, Hugenholtz P, Rabaey K, Tyson GW (2014) Deterministic processes guide long-term synchronised population dynamics in replicate anaerobic digesters. ISME J 8:2015–2028. https://doi.org/10.1038/ismej.2014.50
Wang R, Chen MX, Feng F, Zhang JY, Sui QW, Tong J, Wei YS, Wei DB (2017) Effects of chlortetracycline and copper on tetracyclines and copper resistance genes and microbial community during swine manure anaerobic digestion. Bioresour Technol 238:57–69. https://doi.org/10.1016/j.biortech.2017.03.134
Whiticar MJ (1999) Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chem Geol 161:291–314. https://doi.org/10.1016/S0009-2541(99)00092-3
Wojcieszak M, Pyzik A, Poszytek K, Krawczyk PS, Sobczak A, Lipinski L, Roubinek O, Palige J, Sklodowska A, Drewniak L (2017) Adaptation of methanogenic inocula to anaerobic digestion of maize silage. Front Microbiol 8(1881). https://doi.org/10.3389/fmicb.2017.01881
Yu HG, Wang QY, Wang ZW, Sahinkaya E, Li YL, Ma JX, Wu ZC (2014) Start-up of an anaerobic dynamic membrane digester for waste activated sludge digestion: temporal variations in microbial communities. PLoS One 9:e93710. https://doi.org/10.1371/journal.pone.0093710
Acknowledgements
We would like to thank to Dr. Xijie Yin in the Third Institute of Oceanography of State Oceanic Administration for the help in isotope measurement.
Funding
The study was financially supported by the National Natural Science Foundation of China (51708264), Technology & Science Foundation of Xuzhou (KC16H0228), and Doctoral Scientific Research Foundation of Jiangsu Normal University (15XLR026).
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Lv, Z., Liang, J., Chen, X. et al. Assessment of the start-up process of anaerobic digestion utilizing swine manure: 13C fractionation of biogas and microbial dynamics. Environ Sci Pollut Res 26, 13275–13285 (2019). https://doi.org/10.1007/s11356-019-04703-3
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DOI: https://doi.org/10.1007/s11356-019-04703-3