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The biostimulation of anaerobic digestion with (semi)conductive ferric oxides: their potential for enhanced biomethanation

  • Environmental biotechnology
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Abstract

The effect of biostimulation with ferric oxides, semiconductive ferric oxyhydroxide, and conductive magnetite on the anaerobic digestion of dairy wastewater was examined in a batch mode. The reactors supplemented with ferric oxyhydroxide (R2) and magnetite (R3) showed significantly enhanced biomethanation performance compared with the control (R1). The removal of chemical oxygen demand (COD) after 30 days was 31.9, 59.3, and 82.5 % in R1, R2, and R3, respectively. The consumed COD was almost fully recovered as biogas in R2 and R3, while only 79 % was recovered in R1. The total energy production as biogas was accordingly 32.2, 71.0, and 97.7 kJ in R1, R2, and R3, respectively. The reactors also differed in the acid formation profile with more propionate and butyrate found in R1 and more acetate found in R3. The enhanced biomethanation seems to be associated with variations in the bacterial community structure supposedly induced by the ferric oxides added. In contrast, no evident variation was observed in the archaeal community structure among the reactors. The potential electric syntrophy formed between Methanosaeta concilii-like methanogens and electroactive iron-reducing bacteria, particularly Trichococcus, was likely responsible for the enhanced performance. The stimulated growth of fermentative iron reducers may also have contributed by altering the metabolic characteristics of the bacterial communities to produce more favorable acidogenic products for methanogenesis. The overall results suggest the potential of biostimulation with (semi)conductive ferric oxides to enhance the rate and efficiency of the biomethanation of organic wastes. This seems to be potentially attractive, as increasing attention is being paid to the energy self-sufficiency of waste/wastewater treatment processes today.

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References

  • Ahring BK (2003) Biomethanation I, vol. 1. Springer, New York

    Book  Google Scholar 

  • Akarsubasi AT, Ince O, Kirdar B, Oz NA, Orhon D, Curtis TP, Head IM, Ince BK (2005) Effect of wastewater composition on archaeal population diversity. Water Res 39:1576–1584

    Article  CAS  PubMed  Google Scholar 

  • APHA-AWWA-WEF (2005) Standard Methods for the Examination of Water and Wastewater, 21st edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Baek G, Kim J, Lee C (2014) Influence of ferric oxyhydroxide addition on biomethanation of waste activated sludge in a continuous reactor. Bioresour Technol 166:596–601

    Article  CAS  PubMed  Google Scholar 

  • Bertin L, Lampis S, Todaro D, Scoma A, Vallini G, Marchetti L, Majone M, Fava F (2010) Anaerobic acidogenic digestion of olive mill wastewaters in biofilm reactors packed with ceramic filters or granular activated carbon. Water res 44:4537–4549

    Article  CAS  PubMed  Google Scholar 

  • Caccavo F, Blakemore RP, Lovley DR (1992) A hydrogen-oxidizing, Fe (III)-reducing microorganism from the Great Bay Estuary, New Hampshire. Appl Environ Microbiol 58:3211–3216

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng S, Xing D, Call DF, Logan BE (2009) Direct biological conversion of electrical current into methane by electromethanogenesis. Environ Sci Technol 43:3953–3958

    Article  CAS  PubMed  Google Scholar 

  • Cruz Viggi C, Rossetti S, Fazi S, Paiano P, Majone M, Aulenta F (2014) Magnetite particles triggering a faster and more robust syntrophic pathway of methanogenic propionate degradation. Environ Sci Technol 48:7536–7543

    Article  CAS  PubMed  Google Scholar 

  • De Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K-H, Whitman WB (2009) In: Bergey’s Manual of Systematic Bacteriology, vol Vol. 3: The Firmicutes, 2nd edn. Springer, New York

    Google Scholar 

  • Dinh HT, Kuever J, Muszmann M, Hassel AW, Stratmann M, Widdel F (2004) Iron corrosion by novel anaerobic microorganisms. Nature 427:829–832

    Article  CAS  PubMed  Google Scholar 

  • Fernandez A, Huang S, Seston S, Xing J, Hickey R, Criddle C, Tiedje J (1999) How stable is stable? Function versus community composition. Appl Environ Microbiol 65:3697–3704

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fox JR, Mortimer RJ, Lear G, Lloyd JR, Beadle I, Morris K (2006) The biogeochemical behavior of U (VI) in the simulated near-field of a low-level radioactive waste repository. Appl Geochem 21:1539–1550

    Article  CAS  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: Palaeontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hwang S, Hansen C (1998) Characterization of and bioproduction of short-chain organic acids from mixed dairy-processing wastewater. Trans ASAE 41:795–802

    Article  CAS  Google Scholar 

  • Ivanov VN, Stabnikova EV, Stabnikov VP, Kim IS, Zubair A (2002) Effects of iron compounds on the treatment of fat-containing wastewaters. Appl Biochem Microbiol 38:255–258

    Article  CAS  Google Scholar 

  • Jabari L, Gannoun H, Cayol J-L, Hedi A, Sakamoto M, Falsen E, Ohkuma M, Hamdi M, Fauque G, Ollivier B, Fardeau M-L (2012) Macellibacteroides fermentans gen. Nov., sp. nov., a member of the family Porphyromonadaceae isolated from an upflow anaerobic filter treating abattoir wastewaters. Int J Syst Evol Microbiol 62:2522–2527

    Article  CAS  PubMed  Google Scholar 

  • Kato S, Hashimoto K, Watanabe K (2012) Methanogenesis facilitated by electric syntrophy via (semi)conductive iron-oxide minerals. Environ Microbiol 14:1646–1654

    Article  CAS  PubMed  Google Scholar 

  • Khanal SK, Chen W-H, Li L, Sung S (2004) Biological hydrogen production: effects of pH and intermediate products. Int J Hydrogen Energ 29:1123–1131

    CAS  Google Scholar 

  • Kim J, Jung H, Lee C (2014a) Shifts in bacterial and archaeal community structures during the batch biomethanation of Ulva biomass under mesophilic conditions. Bioresour Technol 169:502–509

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Lee S, Lee C (2013) Comparative study of changes in reaction profile and microbial community structure in two anaerobic repeated-batch reactors started up with different seed sludges. Bioresour technol 129:495–505

    Article  CAS  PubMed  Google Scholar 

  • Kim S-J, Park S-J, Cha I-T, Min D, Kim J-S, Chung W-H, Chae J-C, Jeon CO, Rhee S-K (2014b) Metabolic versatility of toluene-degrading, iron-reducing bacteria in tidal flat sediment, characterized by stable isotope probing-based metagenomic analysis. Environl Microbiol 16:189–204

    Article  CAS  Google Scholar 

  • Kitahara M, Sakamoto M, Tsuchida S, Kawasumi K, Amao H, Benno Y, Ohkuma M (2013) Parabacteroides chinchillae sp. nov., isolated from chinchilla (Chincilla lanigera) feces. Int J Syst Evol Microbiol 63:3470–3474

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Yasuda D, Li Y-Y, Kubota K, Harada H, Yu H-Q (2009) Characterization of start-up performance and archaeal community shifts during anaerobic self-degradation of waste-activated sludge. Bioresour Technol 100:4981–4988

    Article  CAS  PubMed  Google Scholar 

  • Lay J-J, Li Y-Y, Noike T (1998) Developments of bacterial population and methanogenic activity in a laboratory-scale landfill bioreactor. Water Res 32:3673–3679

    Article  CAS  Google Scholar 

  • Lee C, Kim J, Shin SG, O’Flaherty V, Hwang S (2010) Quantitative and qualitative transitions of methanogen community structure during the batch anaerobic digestion of cheese-processing wastewater. Appl Microbiol Biotechnol 87:1963–1973

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Rotaru A-E, Shrestha PM, Malvankar NS, Nevin KP, Lovley DR (2015) Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environ Microbiol 17:648–655

    Article  CAS  PubMed  Google Scholar 

  • Lovely D, Phillips EJP (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540

    Google Scholar 

  • Lovley D (2006) Dissimilatory Fe(III)- and Mn(IV)-Reducing Prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The Prokaryotes. Springer, New York, pp. 635–658

    Chapter  Google Scholar 

  • Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev. 55:259–287

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lovley DR, Phillips EJ, Lonergan DJ (1989) Hydrogen and formate oxidation coupled to dissimilatory reduction of iron or manganese by Alteromonas putrefaciens. Appl Environ Microbiol 55:700–706

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lovley DR, Phillips EJP (1989) Requirement for a microbial consortium to completely oxidize glucose in Fe(III)-reducing sediments. Appl Environ Microbiol 55:3234–3236

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mamais D, Pitt PA, Cheng YW, Loiacono J, Jenkins D (1994) Determination of ferric chloride dose to control struvite precipitation in anaerobic sludge digesters. Water Environ Res 66:912–918

    Article  CAS  Google Scholar 

  • McCune B, Grace JB (2002) Analysis of Ecological Communities. Vol. 2. Glenden Beach, OR: MjM Software Design, USA.

  • Morita M, Malvankar NS, Franks AE, Summers ZM, Giloteaux L, Rotaru AE, Rotaru C, Lovley DR (2011) Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. MBio 2:e00159–e00111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ microbiol 59:695–700

    PubMed Central  CAS  PubMed  Google Scholar 

  • Qu D, Ratering S, Schnell S (2004) Microbial reduction of weakly crystalline iron (III) oxides and suppression of methanogenesis in paddy soil. Bull Environ Contam Toxicol 72:1172–1181

    CAS  PubMed  Google Scholar 

  • Quéméneur M, Hamelin J, Barakat A, Steyer J-P, Carrère H, Trably E (2012) Inhibition of fermentative hydrogen production by lignocellulose-derived compounds in mixed cultures. Int J Hydrogen Energ 37:3150–3159

    Article  Google Scholar 

  • Roden EE, Wetzel RG (2003) Competition between Fe(III)-reducing and methanogenic bacteria for acetate in iron-rich freshwater sediments. Microb Ecol 45:252–258

    Article  CAS  PubMed  Google Scholar 

  • Rotaru A-E, Shrestha PM, Liu F, Shrestha M, Shrestha D, Embree M, Zengler K, Wardman C, Nevin KP, Lovley DR (2014) A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energ Environ Sci 7:408–415

    Article  CAS  Google Scholar 

  • Scott JP (1926) A method of increasing the virulence of Clostridium chauvoei by the use of ferric salts. J Infect Dis 38:511–513

    Article  CAS  Google Scholar 

  • Seifert K, Waligorska M, Wojtowski M, Laniecki M (2009) Hydrogen generation from glycerol in batch fermentation process. Int J Hydrogen Energ 34:3671–3678

    Article  CAS  Google Scholar 

  • Smith KS, Ingram-Smith C (2007) Methanosaeta, the forgotten methanogen? Trends Microbiol 15:150–155

    Article  CAS  PubMed  Google Scholar 

  • Supaphol S, Jenkins SN, Intomo P, Waite IS, O’Donnell AG (2011) Microbial community dynamics in mesophilic anaerobic co-digestion of mixed waste. Bioresour Technol 102:4021–4027

    Article  CAS  PubMed  Google Scholar 

  • Tan H-Q, Li T-T, Zhu C, Zhang X-Q, Wu M, Zhu X-F (2012) Parabacteroides chartae sp. nov., an obligately anaerobic species from wastewater of a paper mill. Int J Syst Evol Microbiol 62:2613–2617

    Article  CAS  PubMed  Google Scholar 

  • Tandukar M, Huber SJ, Onodera T, Pavlostathis SG (2009) Biological chromium (VI) reduction in the cathode of a microbial fuel cell. Environ Sci Technol 43:8159–8165

    Article  CAS  PubMed  Google Scholar 

  • Uchiyama T, Ito K, Mori K, Tsurumaru H, Harayama S (2010) Iron-corroding methanogen isolated from a crude-oil storage tank. Appl Environ Microbiol 76:1783–1788

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ueno Y, Sasaki D, Fukui H, Haruta S, Ishii M, Igarashi Y (2006) Changes in bacterial community during fermentative hydrogen and acid production from organic waste by thermophilic anaerobic microflora. J Appl Microbiol 101:331–343

    Article  CAS  PubMed  Google Scholar 

  • Van Bodegom PM, Scholten JCM, Stams AJM (2004) Direct inhibition of methanogenesis by ferric iron. FEMS Microbiol Ecol 49:261–268

    Article  PubMed  Google Scholar 

  • VandeWalle JL, Goetz GW, Huse SM, Morrison HG, Sogin ML, Hoffmann RG, Yan K, McLellan SL (2012) Acinetobacter, Aeromonas and Trichococcus populations dominate the microbial community within urban sewer infrastructure. Environ Microbiol 14:2538–2552

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Venetsaneas N, Antonopoulou G, Stamatelatou K, Kornaros M, Lyberatos G (2009) Using cheese whey for hydrogen and methane generation in a two-stage continuous process with alternative pH controlling approaches. Bioresour Technol 100:3713–3717

    Article  CAS  PubMed  Google Scholar 

  • Wicher E, Seifert K, Zagrodnik R, Pietrzyk B, Laniecki M (2013) Hydrogen gas production from distillery wastewater by dark fermentation. Intl J Hydrogen Energ 38:7767–7773

    Article  CAS  Google Scholar 

  • Yamada C, Kato S, Ueno Y, Ishii M, Igarashi Y (2015) Conductive iron oxides accelerate thermophilic methanogenesis from acetate and propionate. J Biosci Bioeng 119:678–682

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Chen Y, Zhao Y, Zhu X (2010) New sludge pretreatment method to improve methane production in waste activated sludge digestion. Environ Sci Technol 44:4802–4808

    Article  CAS  PubMed  Google Scholar 

  • Zumstein E, Moletta R, Godon J (2000) Examination of two years of community dynamics in an anaerobic bioreactor using fluorescence polymerase chain reaction (PCR) single-strand conformation polymorphism analysis. Environ Microbiol 2:69–78

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Research Foundation of Korea (NRF) through Basic Science Research Program (2014R1A1A1002329) granted by the Ministry of Science, ICT, and Future Planning and also through International Cooperation Program managed by NRF (2013K2A1A2054369). The authors are also grateful for the support of the Korea Ministry of Environment (MOE) through a Waste-to-Energy Human Resource Development Project.

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Authors and Affiliations

  1. School of Urban and Environmental Engineering, Ulsan National Institute of Science and Technology (UNIST), 50 UNIST-gil, Eonyang-eup, Ulju-gun, Ulsan, 689-798, Republic of Korea

    Gahyun Baek, Jaai Kim & Changsoo Lee

  2. Center for Water Resource Cycle Research, Korea Institute of Science and Technology (KIST), 5 Hwarang-ro 14 gil, Seongbuk-gu, Seoul, 136-791, Republic of Korea

    Kyungjin Cho & Hyokwan Bae

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  1. Gahyun Baek
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  2. Jaai Kim
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  5. Changsoo Lee
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Correspondence to Changsoo Lee.

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Baek, G., Kim, J., Cho, K. et al. The biostimulation of anaerobic digestion with (semi)conductive ferric oxides: their potential for enhanced biomethanation. Appl Microbiol Biotechnol 99, 10355–10366 (2015). https://doi.org/10.1007/s00253-015-6900-y

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