MINI-REVIEW

Factors influencing the degradation of garbagein methanogenic bioreactors and impacts on biogasformation

Masahiko Morita & Kengo Sasaki

Received: 28 November 2011 /Revised: 6 February 2012 /Accepted: 6 February 2012 /Published online: 8 March 2012# Springer-Verlag 2012

Abstract Anaerobic digestion of garbage is attracting muchattention because of its application in waste volume reduc-tion and the recovery of biogas for use as an energy source.In this review, various factors influencing the degradation ofgarbage and the production of biogas are discussed. Thesurface hydrophobicity and porosity of supporting materialsare important factors in retaining microorganisms such asaceticlastic methanogens and in attaining a higher degrada-tion of garbage and a higher production of biogas. Ammoniaconcentration, changes in environmental parameters such astemperature and pH, and adaptation of microbial communityto ammonia have been related to ammonia inhibition. Theeffects of drawing electrons from the methanogeniccommunity and donating electrons into the methanogeniccommunity on methane production have been shown inmicrobial fuel cells and bioelectrochemical reactors. Theinfluences of trace elements, phase separation, andco-digestion are also summarized in this review.

Keywords Anaerobic digestion .Methane fermentation .

Biogas . Garbage

Introduction

Large amounts of garbage (wastes from the food industry,kitchen garbage, etc.) are being produced worldwide, and thus,an efficient treatment system for these wastes is crucial toachieve a recycling-based society (Mata-Alvarez et al. 2000;Montgomery 2004; Yadvika et al. 2004; Haruta et al. 2005;Lee et al. 2009a). Anaerobic digestion such as methanefermentation is attracting much attention for its application inthe treatment and utilization of garbage (Lee et al. 2009a;Angelidaki et al. 2006) because of its low cost, low environ-mental impact, low production of residual sludge, and recoveryof biogas for use as an energy source (Ahring 2003;Forster-Carneiro et al. 2008; Angelidaki et al. 2011).

Methane fermentation normally comprises three reactionphases: hydrolytic–acidogenic, acetogenic, and methano-genic (Ahring 2003; Thauer et al. 2008). Complex organicwastes (carbohydrates, proteins, and lipids) are firstextracellularly degraded into monomers and oligomersby hydrolytic–acidogenic bacteria and then these aretaken up by the bacteria to be further degraded intovolatile fatty acids (VFAs) such as acetate, propionate,and butyrate; hydrogen; carbon dioxide; and alcohols.VFAs such as propionate and butyrate, and alcohols areconverted into acetate, carbon dioxide, and hydrogen byacetogenic bacteria. In the methanogenic phase, methaneis produced from acetate by aceticlastic methanogen andfrom hydrogen/carbon dioxide (CO2) by hydrogenotrophicmethanogen.

Methane fermentation is carried out at various tempera-ture ranges: generally under mesophilic (around 35°C) andthermophilic (around 55°C) conditions and additionally un-der a psychrophilic (4–20°C) or an extreme thermophilic(70°C) condition for the hydrolytic process (Sekiguchi et al.2001; Liu et al. 2008). In methanogenic bioreactors, a

Both authors equally contributed to this work.

M. Morita (*)Biotechnology Sector, Environmental Science ResearchLaboratory, Central Research Institute of Electric Power Industry,1646 Abiko, Abiko-shi,Chiba 270-1194, Japane-mail: masahiko@criepi.denken.or.jp

K. Sasaki (*)Department of Biotechnology, Graduate School of Agriculturaland Life Sciences, The University of Tokyo,Yayoi 1-1-1, Bunkyō,Tokyo 113-8657, Japane-mail: sikengo@gakushikai.jp

Appl Microbiol Biotechnol (2012) 94:575–582DOI 10.1007/s00253-012-3953-z

neutral pH (6.6–7.6) is usually maintained because thisis the preferred pH range of methanogenic archaea.

To attain high loading and stable methanogenesis,approaches such as the use of a two-stage system, apacked-bed or fixed-bed system, additives such as inorganicelements, and co-digestion with other organic wastes areused for garbage treatment (Mata-Alvarez et al. 2000;Yadvika et al. 2004; Tatara et al. 2004, 2008; Angelidakiet al. 2006; Sasaki et al. 2006, 2007; Ueno et al. 2007a;Umaña et al. 2008). The aim of this review is to describesuch approaches that influence the degradation of gar-bage and the production of methane gas. Special focusis given to the effect of the relation between electronbalance and the microbial communities in the methanogenicbioreactor.

Retention of microorganisms by using supportingmaterials

Immobilization of microbial consortia is important forthe optimum operation of an anaerobic treatment sys-tem because it prevents the accidental washout ofmicroorganisms. Anaerobic treatment systems that areused with supporting materials include the fixed-bed,packed-bed, and fluidized-bed reactors. A variety ofmaterials, such as carbon fiber, glass, polyethylene fi-ber, and zeolite filter, are used for the degradation ofgarbage or garbage leachate (Ueno et al. 2007a; Castillaet al. 2009; Sasaki et al. 2010a; Zhang et al. 2011). Inaddition, clay fiber, polypropylene membrane, polyure-thane foam, polyvinyl-chloride sheets, and tire rubberare used as supporting materials for wastewater treat-ment (Wilkie and Colleran 1984; Show and Tay 1999;Picanço et al. 2001; Tatara et al. 2004; Chauhan andOgram 2005; Umaña et al. 2008). The types and char-acteristics of supportingmaterials are summarized in Table 1.

Previous reports showed that retaining a high number ofmicro-organisms in a carbon fiber supporting material (Fig. 1) en-hanced the digestibility of garbage slurry even at high organicloading rates (Ueno et al. 2007a; Sasaki et al. 2009). Additionof supporting materials also shortens the start-up period(Wilkie and Colleran 1984; Sasaki et al. 2009). Previousresearchers have performed shredding of the substrate toprevent clogging (Ueno et al. 2007a; Sasaki et al.2009). Zeolite also plays a role in improving microbialactivity by supplementing trace elements (Castilla et al.2009).

Previous analyses on wastewaters and garbage have dem-onstrated that the physical characteristics of the supportingmaterial influence its ability to retain microorganisms. Sur-face hydrophobicity is an important factor for the attach-ment of microorganisms to the supporting material (Pringleand Fletcher 1983; Van Pelt et al. 1985; Sasaki et al. 2010a)and has an effect on methanogenesis by syntrophic–meth-anogenic consortia (Chauhan and Ogram 2005). In addition,supporting materials having a porous structure have beenshown to retain high total microbial numbers (Show and Tay1999; Picanço et al. 2001). A higher porosity is related to ahigher removal of organic wastes and/or a higher productionof methane (Show and Tay 1999; Sasaki et al. 2010a).Aceticlastic methanogens form colonies well in or on aporous supporting material, thereby leading to an efficientremoval of acetate (Picanço et al. 2001; Sasaki et al. 2006).In a previous study, a supporting material with surfacehydrophobicity and a porous structure enhanced the decom-position of rice straw probably by retaining hydrogenotro-phic methanogens near cellulolytic bacteria (Sasaki et al.2010b), as scavenging hydrogen is advantageous for degra-dation of cellulose (Robert et al. 2001). In addition, efficientremoval of hydrogen and/or formate is essential for obligatesyntrophic decomposition of VFAs such as butyrate andpropionate (Dong et al. 1994; Imachi et al. 2007; Stamsand Plugge 2009).

Table 1 Supporting material types and their characteristics

Supporting material Surface characteristics Other characteristics Reference

Carbon fiber textiles Hydrophobic Porous structure, surface protrusion Tatara et al. (2008)

Clay fiber Hydrophilic Porous structure Wilkie and Colleran (1984)

Glass Hydrophilic Sasaki et al. (2010a)

Polyethylene fiber Hydrophobic Porous structure Sasaki et al. (2010a)

Polypropylene membrane Hydrophobic Porous structure Chauhan and Ogram (2005)

Polyurethane foam Hydrophobic Porous structure Picanço et al. (2001)

Polyvinyl-chloride sheet Hydrophobic Porous structure Show and Tay (1999)

Tire rubber Hydrophobic Porous structure Umaña et al. (2008)

Zeolite filter Hydrophilic Porous structure, cation exchange,supplementing trace element

Umaña et al. (2008)

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Ammonia inhibition

Ammonia (NH4+/NH3) is produced during the degradation of

nitrogenous materials (Kayhanian 1999). Although ammoniais essential for microbial growth, an excess of free (un-ion-ized) ammonia (NH3) causes inhibition of anaerobic diges-tion. Studies about ammonia inhibition against methanogenicarchaea suggested that (1) ammonium ions directly inhibit themethane-synthesizing enzymes, and (2) ammonia that passesinto the cell is toxic and causes proton imbalance and/orpotassium deficiency (Sprott et al. 1984; Sprott and Patel1986; Gallert et al. 1998; Sung and Liu 2003). The freeammonia concentration increases as the total ammonia con-centration (NH4

+ + NH3), temperature, and pH increase(McCarty and McKinney 1961; Braun et al. 1981; Koster1986; Angelidaki and Ahring 1994). An increase in carbondioxide pressure, and thereby a lowering of pH, can decreasethe inhibitory effect of free ammonia (Vavilin et al. 1995).

In addition to the free ammonia concentration andchanges in environmental parameters (temperature andpH), adaptation of the microorganisms to ammonia is alsorelated to ammonia inhibition (Table 2). In an unadaptedprocess, ammonia inhibition occurred at 0.08–0.15 gN/l freeammonia concentration (Braun et al. 1981; de Baere et al.1984; Ikbal et al. 2003), while an adapted inhibition during

the treatment of livestock manure occurred at 0.7–1.1 gN/l of free ammonia (Angelidaki and Ahring 1993; Hansen etal. 1998). The total ammonia concentration is also a factor inthe inhibition of methanogenesis (Zeeman et al. 1985). Withunadapted cultures, ammonia inhibition occurred at a totalammonia concentration of about 2.5 gN/l (van Velsen 1979;Hashimoto 1986), while adapted cultures can tolerate am-monia up to a concentration of 4–6.5 gN/l (Hashimoto1986; Angelidaki and Ahring 1993; Schnürer et al. 1999).In a previous study with an unadapted sludge, ammoniainhibition during the degradation of artificial garbage slurrywas observed at 0.29 gN/l free ammonia and 1.5 gN/l totalammonia (Sasaki et al. 2011a).

Chen et al. (2008) reviewed various methods used tocounteract ammonia inhibition, including adaptation. Twopractical methods were tested successfully: (1) dilution ofthe reactor contents with water and (2) adjustment of feed-stock C/N ratio (Kayhanian 1999). Physicochemical or bio-logical removal of ammonia from methanogenic sludge isanother approach. Physicochemical methods include ammo-nia stripping (Abouelenien et al. 2010), chemical precipita-tion with magnesium ammonium phosphate (Demeestere etal. 2001), and selective exchange of ammonium ions byusing zeolite or glauconite (Borja et al. 1993; Hansen et al.1999). Biological processes in sequential anaerobic, aero-bic/anoxic, or anaerobic multi-compartment systems includenitrification/denitrification and anaerobic ammonia oxida-tion (Baloch et al. 2006; Agdag and Sponza 2008; Bernetand Béline 2009). Addition of clay (as a mineral supply andfor biomass retention), activated carbon (for sulfide removaland biomass retention), carbon fiber textiles (for biomassretention), or FeCl2 (for sulfide removal) and increasinghydraulic retention time (for biomass retention) are alsoeffective for counteracting ammonia inhibition (Borja et al.1996; Hansen et al. 1999; Sasaki et al. 2011a). Magnesiumand calcium were shown to be somewhat antagonistic toammonia inhibition (McCarty and McKinney 1961).

Fig. 1 Carbon fiber supporting material. The bar is 1 mm for themicroscopic image

Table 2 Various parameters involved in ammonia inhibition on methanogenesis

Free NH3a (g N/l) Total NH3

a (g N/l) pH Temperature (°C) Adaptation Substrate Reference

0.15 – 6.5–7.5 37 Unadapted Piggery manure Braun et al. (1981)

0.08–0.10 7.9 7.0 35 Unadapted Medium containing NH4Cl de Baere et al. (1984)

0.03–0.05 2.4 7.2–7.4 30 Unadapted Medium containing NH4Cl van Velsen (1979)

0.10–0.15 1.0–2.0 7.8 37 Unadapted Medium containing (NH4)2HPO4 Ikbal et al. (2003)

0.20 2.5 7.4 55 Unadapted Beef manure containing NH4Cl Hashimoto (1986)

0.29 1.5 7.8 55 Unadapted Garbage containing NH4Cl Sasaki et al. (2011a)

0.53 6.5 7.8 37 Adapted Slaughterhouse waste Schnürer et al. (1999)

1.10 4.1 8.0 55 Adapted Swine manure+NH4Cl Hansen et al. (1998)

0.39 4.0 7.4 55 Adapted Beef manure containing NH4Cl Hashimoto (1986)

a Concentrations of free ammonia and total ammonia were calculated according to Hashimoto (1986) and Garcia and Angenent (2009)

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Conflicting information exists about the tolerance ofmethanogens to ammonia. Hydrogenotrophic methanogenswere reported to be more tolerant to free ammonia thanaceticlastic methanogens under thermophilic conditions(Angelidaki and Ahring 1993; Sasaki et al. 2011a). Support-ing materials prevent ammonia inhibition and acetate accu-mulation by proliferating aceticlastic methanogens in theinner region, although hydrogenotrophic methanogens cangrow even in suspended fractions at a free ammonia level of0.29 gN/l (Sasaki et al. 2011a). However, Wiegant andZeeman (1986) observed that hydrogenotrophic methano-gens were more sensitive to ammonia than aceticlasticmethanogens. Research evidence also shows that syntrophicdecomposition by acetate-oxidizing bacteria and hydroge-notrophic methanogens dominate in mesophilic conditionsunder high ammonia levels (Schnürer and Nordberg 2008).

Relation between electron balanceand the methane-producing bacterialcommunity

Electron exchange, such as interspecies hydrogen or formatetransfer, occurs in methanogenic systems (Stams and Plugge2009; McInerney et al. 2009). A variety of organic com-pounds can be reduced to produce hydrogen and/or formate,which the methanogens consume. Methanogens have beenreported to be able to accept electron directly in aggregates(Morita et al. 2011). Therefore, a direct or indirect electrontransfer between microorganisms is essential for methaneproduction. Disrupting the electron balance in methanogenicsystems by using microbial fuel cells (MFCs) (Jung andRegan 2011) or a bioelectrochemical reactor (BER)(Fig. 2) (Sasaki et al. 2010c) has been shown to influencemethane production.

Drawing electrons from the methanogenic community

The effect of drawing electrons on methane production canbe gained using MFCs. MFCs produce a difference in po-tential between the anodic and cathodic electrodes in orderto extract electricity (Logan et al. 2006; Lovley 2006). In theanodic chamber of an MFC, reduced materials are oxidizedand electrons are transferred to the anode under an anoxiccondition. Protons simultaneously generated in the anodicchamber are transferred to the cathodic chamber through amembrane. Electrogenesis occurs when soluble electronacceptors such as oxygen, nitrate, and sulfate are not abun-dantly present, and therefore, electrogenesis can potentiallycompete with methanogenesis (Ishii et al. 2008). Oncemethane-producing microorganisms become established,electrogenesis will be difficult to induce (Ishii et al. 2008).However, the transfer and enrichment of anode-grown

biofilms (Kim et al. 2005), the predominance of metal-reducing bacteria such as Geobacter (Bond and Lovley2003) and Shewanella spp. (Gorby et al. 2006), and processoptimization by, for example, cathode modification (Loganet al. 2006) can increase the generation of electricity. Redoxpotential is suggested to be one of the factors that affect thecompetition between electrogenesis and methanogenesis. Inan acetate-fed MFC, methane production is lower at higheranodic potentials. A previous result showing that the anodicreaction suppressed methane production in a methane fer-mentor degrading complex organic materials correspondedwith the above results (Sasaki et al. 2011b). However, in aglucose-fed MFC, methanogenesis was not affected by theanodic potential, and other factors might have influenced thecompetition (Jung and Regan 2011).

Donating electrons into the methanogenic community

Abundant information is available about the effect of donat-ing electrons on methane production by using a BER. ABER has similar circuitry as an MFC system. It can controlelectric flow and influence microbial metabolism (Thrashand Coates 2008) and is also known to indirectly or directlytransfer electrons to microorganisms.

For indirect electron transfer, electron shuttles efficientlycarry electrons from the cathodic electrode to the micro-organisms. Addition of neutral red to methanogenic gran-ules in the cathodic compartment of a BER has been shownto increase methane production from carbon dioxide (Park et

Fig. 2 H-type bioelectrochemical reactor. Left and right sides arecathodic and anodic chambers, respectively

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al. 1999). The Eo′ of neutral red (−0.325 V versus thestandard hydrogen electrode [SHE]) is similar to that ofNADH (−0.320 V versus SHE), and neutral red might playa role in reducing power for energy conservation of micro-organisms (Park et al. 1999). A previous result has shownthat the cathodic reaction in the methane fermentor withanthroquinone-2.6-disulfonate (Eo′ 0 −0.184 V versusSHE) stabilized methane production at high organic loadingrates and prevented accumulation of VFAs (Sasaki et al.2010c). Inhibition of methanogenesis by methyl viologen(Eo′ 0 −0.450 V versus SHE) has also been reported (Wolinet al. 1964).

In addition to electron shuttles, electrons can also bemediated by hydrogen produced from water electrolysis.At pH 7, the Eo′ of hydrogen is −0.450 V versus SHE.Through microbial activity, electrochemically producedhydrogen at the cathode could be converted to methane(Clauwaert et al. 2008).

Microorganisms can directly accept electron from thecathode, as exemplified by Geobacter sp. (Gregory et al.2004). In previous studies, a biofilm attached on the cathodeand composed mainly of hydrogenotrophic methanogensproduced methane directly from current (Cheng et al.2009; Villano et al. 2010).

Influence of trace elements

Supplementation of trace elements such as nickel, cobalt,iron, zinc, molybdenum, and/or tungsten has a strong impacton anaerobic treatment of wastewater (Takashima andSpeece 1990). These trace elements are related to the activ-ity of the enzymes in methanogenic systems (Takashima andSpeece 1990). Many studies have reported that the additionof a single trace element or combinations of different traceelements to a methane fermentor improves reactor perfor-mance, with respect to specific substrate removal, lowerVFA concentration, and higher gas production (Murrayand van den Berg 1981; Takashima and Speece 1989; Jarviset al. 1997; Kida et al. 2001; Osuna et al. 2003; Zandvoort etal. 2006; Worm et al. 2009; Pobeheim et al. 2010). Thereby,organic loading rates can be increased (Jarvis et al. 1997;Kida et al. 2001). The concentration of the trace elementsused differed among studies, probably owing to the differentcharacteristics of the substrate used.

In addition to wastewater treatment, supplementation oftrace elements (iron, nickel, and cobalt) was shown to beeffective for propionate removal in a reactor degradingcomplex organic materials such as dog food, despite thesubstrate having enough nutrients (Kim et al. 2002). Sup-plementation of nickel and cobalt was also shown to in-crease the levels of the methanogenic enzymes coenzymeF430 and corrinoid in an acetate-degrading reactor (Kida et

al. 2001) and to induce syntrophic degradation by bacteriaand methanogens in a protein-degrading reactor, which isenergetically more efficient than degradation by a singlespecies (Tang et al. 2005). F430 and corrinoid were consid-ered to be involved in methane production from methyl-S-coenzyme M and methyl transfer to H-S-coenzyme M,respectively (Friedmann et al. 1990; Gottschalk and Thauer2001). Nickel and cobalt were also effective for the start-upof methane production in the bioreactor degrading dog food(our unpublished data).

Phase separation

A two-stage process involving an acidogenic and a methano-genic phase is effective for higher methane production fromgarbage (Feng et al. 2008; Ueno et al. 2007a). In such aprocess, the fermentation products (VFAs) are converted tomethane-containing gas. It was reported that a two-stageprocess could attain a higher organic loading rate and a highermethane production from garbage and is less vulnerable tofluctuations in organic loading rate than a single methano-genic process (Ueno et al. 2007b; Park et al. 2008). In theacidogenic phase, hydrogen is obtained as a by-product (Leeet al. 2010). To suppress methanogenic activity and favorhydrogen production in hydrogen fermentation, various oper-ational conditions were applied, including heat treatment ofthe inoculum and optimization of operating conditions such ashydraulic retention time, pH (4.5–6.0), temperature, and sub-strate concentration (Hawkes et al. 2007). Koike et al. (2009)applied a two-stage process consisting of a saccharificationand fermentation stage and a dry methane fermentation stageto obtain ethanol and methane from garbage.

Co-digestion

Co-digestion was also shown to be effective, although thesubstrate mixture should be appropriately regulated for op-timal operation as to C/N ratio; moisture; pH; concentrationsof nutrients, inhibitors, toxic compounds, biodegradableorganic matter, and dry matter; and other factors (Mata-Alvarez et al. 2011). Kitchen garbage was efficientlydigested by the addition of excess sludge from biologicalsewage treatment processes (Kim et al. 2003; Lee et al.2009b). Co-digestion with garbage improved the digestionof swine manure and daily cattle manure even though thepercentage of garbage was only 2–3% (Liu et al. 2009).

Acknowledgment This work was supported in part by the NewEnergy and Industrial Technology Development Organization (NEDO)of Japan.

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