Skip to main content

Advertisement

Log in

Effects of heavy metals as stress factors on anaerobic digestion processes and biogas production from biomass

  • Review
  • Published:
International Journal of Environmental Science and Technology Aims and scope Submit manuscript

Abstract

Heavy metals affect the biochemical reactions that take place during anaerobic digestion processes of organic matter. In this review, the different effects observed in anaerobic digestion processes and during the production of biomethane and biohydrogen from several substrates contaminated with and/or inheriting heavy metals from the substrates themselves were discussed. It has been found that heavy metals exert important roles in biochemical reactions. Heavy metals like copper, nickel, zinc, cadmium, chromium and lead have been overwhelmingly reported to be inhibitory and under certain conditions toxic in biochemical reactions depending on their concentrations. Heavy metals like iron may also exhibit stimulatory effects, but these effects have been scantily observed. This review also concludes that the severity of heavy metal inhibition depends upon factors like metal concentration in a soluble, ionic form in the solution, type of metal species, and amount and distribution of biomass in the digester or chain of biochemical reactions which constitute the anaerobic digestion process. A majority of studies have demonstrated that the toxic effect of heavy metals like chromium, cadmium and nickel is attributable to a disruption of enzyme function and structure by binding of the metal ions with thiol and other groups on protein molecules or by replacing naturally occurring metals in enzyme prosthetic groups. This review has not found published data on the effects of heavy metals on the hydrolysis stage of anaerobic digestion process chemistry, and hence further studies are required to depict any changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Akila G, Chandra TS (2007) Performance of an UASB reactor treating synthetic wastewater at low-temperature using cold-adapted seed slurry. Process Biochem 42:466–471

    Article  CAS  Google Scholar 

  • Angelidaki I, Ahring BK (1994) Anaerobic digestion of manure at different ammonia loads: effect of temperature. Wat Res 28:727–731

    Article  CAS  Google Scholar 

  • Angelidaki I, Alves M, Bolzonella D, Borzacconi L, Campos JL, Guwy AJ, Kalyuzhnyi S, Jenicek P, van Lier JB (2009) Defining the biomethane potential (BMP) of solid organic wastes and energy crops: a proposed protocol for batch assays. Wat Sci Technol 59:927–934

    Article  CAS  Google Scholar 

  • Appels L, Lauwers J, Degrève J, Helsen L, Lievens B, Willems K, Impe JV, Dewil R (2011) Anaerobic digestion in global bio-energy production: potential and research challenges. Renew Sust Energy Revi 15:4295–4301

    Article  CAS  Google Scholar 

  • Argun H, Kargi F, Kapdan IK (2009) Microbial culture selection for bio-hydrogen production from waste ground wheat by dark fermentation. Int J Hydrogen Energy 34:2195–2200

    Article  CAS  Google Scholar 

  • Aziz MA, Ng WN, Jinadasa KBSN (2004) Inhibitory effects of zinc on acidogenic–anaerobic biotreatment of wastewaters. IE(I) J–EN 84:39–42

    Google Scholar 

  • Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations: a review. Wat Air Soil Pollut 47:335–379

    Article  Google Scholar 

  • Bartacek J, Fermoso FG, Baldo-Urrutia AM, van Hullebusch ED, Lens PNL (2008) Cobalt toxicity in anaerobic granular sludge: influence of chemical speciation. J Ind Microbiol Biotechnol 35:1465–1474

    Article  CAS  Google Scholar 

  • Bayer EA, Lamed R, Himmel ME (2007) The potential of cellulases and cellulosomes for cellulosic waste management. Curr Opin Biotechnol 18:237–245

    Article  CAS  Google Scholar 

  • Bertin L, Bettini C, Zanaroli G, Fraraccio S, Negroni A, Fava F (2012) Acclimation of an anaerobic consortium capable of effective biomethanization of mechanically-sorted organic fraction of municipal solid waste through a semi-continuous enrichment procedure. J Chem Technol Biotechnol 87:1312–1319

    Google Scholar 

  • Bouallagui H, Haouari O, Touhami Y, Cheikh RB, Marouani L, Hamdi M (2004) Effect of temperature on the performance of an anaerobic tubular reactor treating fruit and vegetable waste. Process Biochem 39:2143–2148

    Article  CAS  Google Scholar 

  • Brady D, Duncan JR (1994) Binding of heavy metals by the cell walls of Saccharomyces cerevisiae. Enzym Microbiol Technol 16:633–638

    Article  CAS  Google Scholar 

  • Capone DG, Reese DD, Kiene RP (1983) Effects of metals on methanogenesis; sulfate reduction; carbon dioxide evolution; and microbial biomass in anoxic salt marsh sediments. Appl Environ Microbiol 45:1586–1591

    CAS  Google Scholar 

  • Chandra R, Venkata Mohan S (2011) Microalgal community and their growth conditions influence biohydrogen production during integration of dark-fermentation and photo-fermentation processes. Int J Hydrogen Energy 36:12211–12219

    Article  CAS  Google Scholar 

  • Chang BV, Lu ZJ, Yuan SY (2009) Anaerobic degradation of nonylphenol in subtropical mangrove sediments. J Hazard Mater 165:162–167

    Article  CAS  Google Scholar 

  • Chen SF, Yakunin AF, Kuznetsova E, Busso D, Pufan R, Proudfoot M, Kim R, Kim SH (2004) Structural and functional characterization of a novel phosphodiesterase from Methanococcus jannaschii. J Biol Chem 279:31854–31862

    Article  CAS  Google Scholar 

  • Chen Y, Cheng JJ, Creamer KS (2008a) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99:4044–4064

    Article  CAS  Google Scholar 

  • Chen SD, Lee KS, Lo YC, Chen WM, Wu JF, Lin CY, Chang JS (2008b) Batch and continuous biohydrogen production from starch hydrolysate by Clostridium species. Int J Hydrogen Energy 33:1803–1812

    Article  CAS  Google Scholar 

  • Chong ML, Rahim RA, Shirai Y, Hassan MA (2009) Biohydrogen production by Clostridium butyricum EB6 from palm oil mill effluent. Int J Hydrogen Energ 34:764–771

    Article  CAS  Google Scholar 

  • Chynoweth DP, Owens JM, Legrand R (2001) Renewable methane from anaerobic digestion of biomass. Renewable Energy 22:1–8

    Article  CAS  Google Scholar 

  • Cirne DG, Paloumet X, Bjornsson L, Alves MM, Mattiasson B (2007) Anaerobic digestion of lipid-rich waste: effects of lipid concentration. Renewable Energy 32:965–975

    Article  CAS  Google Scholar 

  • Codina JC, Ascensión Muñoz M, Cazorla FM, Pérez-García A, Moriñigo MA, De Vicente A (1998) The inhibition of methanogenic activity from anaerobic domestic sludges as a simple toxicity bioassay. Wat Res 32:1338–1342

    Article  CAS  Google Scholar 

  • Colussi I, Cortesi A, Della Vedova L, Gallo V, Cano Robles FK (2009) Start-up procedures and analysis of heavy metals inhibition on methanogenic activity in EGSB reactor. Bioresour Technol 100:6290–6294

    Article  CAS  Google Scholar 

  • Demirel B, Scherer P (2011) Trace element requirements of agricultural biogas digesters during biological conversion of renewable biomass to methane. Biomass Bioenergy 35:992–998

    Article  CAS  Google Scholar 

  • Demirel B, Yenigun O (2004) Anaerobic acidogenesis of dairy wastewater: the effects of variations in hydraulic retention time with no pH control. J Chem Technol Biotechnol 79:755–760

    Article  CAS  Google Scholar 

  • Demirel B, Yenigün O (2002) Two-phase anaerobic digestion processes: a review. J Chem Technol Biotechnol 77:743–755

    Article  CAS  Google Scholar 

  • El-Mashad HM, Zeeman G, Van Loon WKP, Bot GPA, Lettinga G (2004) Effect of temperature and temperature fluctuation on thermophilic anaerobic digestion of cattle manure. Bioresour Technol 95:191–201

    Article  CAS  Google Scholar 

  • Elmitwalli TA, Otterpohl R (2007) Anaerobic biodegradability and treatment of grey water in upflow anaerobic sludge blanket (UASB) reactor. Wat Res 41:1379–1387

    Article  CAS  Google Scholar 

  • Fan KS, Kan NR, Lay JJ (2006) Effect of hydraulic retention time on anaerobic hydrogenesis in CSTR. Bioresour Technol 97:84–89

    Article  CAS  Google Scholar 

  • Fang HHP (1997) Inhibition of bioactivity of UASB biogranules by electroplating metals. Pure Appl Chem 69:2425–2429

    Article  CAS  Google Scholar 

  • Fang HHP, Chan OC (1997) Toxicity of electroplating metals on benzoate-degrading granules. Environ Technol 18:93–99

    Article  CAS  Google Scholar 

  • Fang HHP, Hui HH (1994) Effect of heavy metals on the methanogenic activity of starch-grading granules. Biotechnol Lett 16:1091–1096

    Article  CAS  Google Scholar 

  • Fang HHP, Yu HQ (2000) Effect of HRT on mesophilic acidogenesis of dairy wastewater. J Environ Eng 126:1145–1148

    Article  CAS  Google Scholar 

  • Fantozzi F, Buratti C (2009) Biogas production from different substrates in an experimental continuously stirred tank reactor anaerobic digester. Bioresour Technol 100:5783–5789

    Article  CAS  Google Scholar 

  • Ferrer I, Ponsá S, Vázquez F, Font X (2008) Increasing biogas production by thermal (70 °C) sludge pre-treatment prior to thermophilic anaerobic digestion. Biochem Eng J 42:186–192

    Article  CAS  Google Scholar 

  • Funk T, Gu WW, Friedrich S, Wang HX, Gencic S, Grahame DA, Cramer SP (2004) Chemically distinct Ni sites in the A-cluster in subunit beta of the acetyl-CoA decarbonylase/synthase complex from Methanosarcina thermophila:NiL-edge absorption and X-ray magnetic circular dichroism analyses. J Am Chem Soc 126:88–95

    Article  CAS  Google Scholar 

  • Giotta L, Agostiano A, Italiano F, Milano F, Trotta M (2006) Heavy metal ion influence on the photosynthetic growth of Rhodobacter sphaeroides. Chemosphere 62:1490–1499

    Article  CAS  Google Scholar 

  • Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21:383–393

    Article  CAS  Google Scholar 

  • Gonzalez-Gil G, Kleerebezem R, Lettinga G (1999) Effects of nickel and cobalt on kinetics of methanol conversion by methanogenic sludge as assessed by on-line CH4 monitoring. Appl Environ Microbiol 65:1789–1793

    CAS  Google Scholar 

  • Gonzalez-Silva BM, Briones-Gallardo R, Razo-Flores E, Celis LB (2009) Inhibition of sulfate reduction by iron; cadmium and sulfide in granular sludge. J Hazard Mater 172:400–407

    Article  CAS  Google Scholar 

  • Hartmann H, Ahring BK (2005) Anaerobic digestion of the organic fraction of municipal solid waste: influence of co-digestion with manure. Wat Res 39:1543–1552

    Article  CAS  Google Scholar 

  • Hickey RF, Vaderwielen J, Switzenbaum MS (1989) The effect of heavy metals on methane production and hydrogen and carbon monoxide levels during batch anaerobic sludge digestion. Wat Res 23:207–218

    Article  CAS  Google Scholar 

  • Jackson WA, Pardue JH (1998) Assessment of metal inhibition of reductive dechlorination of hexachlorobenzene at a superfund site. Environ Toxicol Chem 17:1441–1446

    Article  CAS  Google Scholar 

  • Jackson-Moss CA, Duncan JR, Cooper DR (1989) The effect of calcium on anaerobic digestion. Biotechnol Lett 11:219–224

    Article  CAS  Google Scholar 

  • Jain SK, Gujral GS, Jha NK, Vasudevan P (1992) Production of biogas from Azolla pinnata R.Br and Lemna minor L.: effect of heavy metal contamination. Bioresour Technol 41:273–277

    Article  CAS  Google Scholar 

  • Jeong E, Kim HW, Nam JY, Shin HS (2010) Enhancement of bioenergy production and effluent quality by integrating optimized acidification with submerged anaerobic membrane bioreactor. Bioresour Technol 101:7–12

    Article  CAS  Google Scholar 

  • Jo JH, Lee DS, Park D, Park JM (2008) Biological hydrogen production by immobilized cells of Clostridium tyrobutyricum JM1 isolated from a food waste treatment process. Bioresour Technol 99:6666–6672

    Article  CAS  Google Scholar 

  • Kapdan IK, Kargi F, Oztekin R, Argun H (2009) Bio-hydrogen production from acid hydrolyzed wheat starch by photo-fermentation using different Rhodobacter sp. Int J Hydrogen Energy 34:2201–2207

    Article  CAS  Google Scholar 

  • Kavamura VN, Esposito E (2010) Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol Adv 28:61–69

    Article  CAS  Google Scholar 

  • Khanal SK (2008) Overview of anaerobic biotechnology, Chapter 1, In: anaerobic biotechnology for bioenergy production: principles and applications, Wiley and Blackwell Publishing, pp 1–27

  • Kim M, Ahn YH, Speece RE (2002) Comparative process stability and efficiency of anaerobic digestion: mesophilic versus thermophilic. Wat Res 36:4369–4385

    Article  CAS  Google Scholar 

  • Kim JK, Oh BR, Chun YN, Kim SW (2006) Effects of temperature and hydraulic retention time on anaerobic digestion of food waste. J Biosci Bioeng 102:328–332

    Article  CAS  Google Scholar 

  • Kotsopoulos TA, Zeng RJ, Angelidaki I (2006) Biohydrogen production in granular up-flow anaerobic sludge blanket (UASB) reactors with mixed cultures under hyper-thermophilic temperature (70 °C). Biotechnol Bioeng 94:296–302

    Article  CAS  Google Scholar 

  • Kumar A, Miglani P, Gupta RK, Bhattacharya TK (2006) Impact of Ni(II); Zn(II) and Cd(II) on biogasification of potato waste. J Environ Biol 27:61–66

    CAS  Google Scholar 

  • Kuntze K, Kiefer P, Baumann S, Seifert J, von Bergen M, Vorholt JA, Boll M (2011) Enzymes involved in the anaerobic degradation of meta-substituted halobenzoates. Mol Microbiol 82:758–769

    Article  CAS  Google Scholar 

  • Kuo CW, Genthner BRS (1996) Effect of added heavy metal ions on biotransformation and biodegradation of 2-chlorophenol and 3-chlorobenzoate in anaerobic bacterial consortia. Appl Environ Microbiol 62:2317–2323

    CAS  Google Scholar 

  • Lang XM, Shi XC, Wang GG (2007) New micro-electrolytic and bio-enhancing processing technology in treating nitrobenzene sewage. J Saf Environ 7:66

    Google Scholar 

  • Leighton IR, Forster CF (1998) The effect of heavy metals on a thermophilic methanogenic upflow sludge blanket reactor. Bioresour Technol 63:131–137

    Article  CAS  Google Scholar 

  • Li C, Fang HHP (2007) Inhibition of heavy metals on fermentative hydrogen production by granular sludge. Chemosphere 67:668–673

    Article  CAS  Google Scholar 

  • Liew LN, Shi J, Li Y (2011) Enhancing the solid-state anaerobic digestion of fallen leaves through simultaneous alkaline treatment. Bioresour Technol 102:8828–8834

    Article  CAS  Google Scholar 

  • Lin CY (1992) Effect of heavy metals on volatile fatty acid degradation in anaerobic digestion. Wat Res 26:177–183

    Article  CAS  Google Scholar 

  • Lin CY (1993) Effect of heavy metals on acidogenesis in anaerobic digestion. Wat Res 27:147–152

    Article  CAS  Google Scholar 

  • Lin CY, Chen CC (1999) Effect of heavy metals on the methanogenic UASB granule. Wat Res 33:409–416

    Article  CAS  Google Scholar 

  • Lin CY, Shei SH (2008) Heavy metal effects on fermentative hydrogen production using natural mixed microflora. Int J Hydrogen Energy 33:587–593

    Article  CAS  Google Scholar 

  • Lin CY, Chou J, Lee YS (1998) Heavy metal-affected degradation of butyric acid in anaerobic digestion. Bioresour Technol 65:159–161

    Article  CAS  Google Scholar 

  • Lins P, Reitschuler C, Illmer P (2012) Development and evaluation of inocula combating high acetate concentrations during the start-up of an anaerobic digestion. Bioresour Technol 110:167–173

    Article  CAS  Google Scholar 

  • Liu DW, Liu DP, Zeng RJ, Angelidaki I (2006) Hydrogen and methane production from household solid waste in the two-stage fermentation process. Wat Res 40:2230–2236

    Article  CAS  Google Scholar 

  • Lo HM, Chiang CF, Tsao HC, Pai TY, Liu MH, Kurniawan TA, Chao KP, Liou CT, Lin KC, Chang CY, Wang SC, Banks CJ, Lin CY, Liu WF, Chen PH, Chen CK, Chiu HY, Wu HY, Chao TW, Chen YR, Liou DW, Lo FC (2012) Effects of spiked metals on the MSW anaerobic digestion. Waste Manag Res 30:32–48

    Article  CAS  Google Scholar 

  • Lovley DR, Nevin KP (2011) A shift in the current: new applications and concepts for microbe-electrode electron exchange. Curr Opin Biotechnol 22:441–448

    Article  CAS  Google Scholar 

  • Ludden PW, Robert GP (1995) The biochemistry and genetics of nitrogen fixation by photosynthetic bacteria. In: Blankenship BE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, pp 929–947

    Google Scholar 

  • Luostarinen S, Rintala J (2007) Anaerobic on-site treatment of kitchen waste in combination with black water in UASB-septic tanks at low temperatures. Bioresour Technol 98:1734–1740

    Article  CAS  Google Scholar 

  • Massé D, Gilbert Y, Topp E (2011) Pathogen removal in farm-scale psychrophilic anaerobic digesters processing swine manure. Bioresour Technol 102:641–646

    Article  CAS  Google Scholar 

  • Mata-Alvarez J, Macé S, Llabrés P (2000) Anaerobic digestion of organic solid wastes. An overview of research achievements and perspectives. Bioresour Technol 74:3–16

    Article  CAS  Google Scholar 

  • Mishra SR, Bharati K, Sethunathan N, Adhya TK (1999) Effects of heavy metals on methane production in tropical rice soils. Ecotoxicolo Environ Saf 44:129–136

    Article  CAS  Google Scholar 

  • Nadais H, Capela I, Arroja L, Duarte A (2005) Treatment of dairy wastewater in UASB reactors inoculated with flocculent biomass. Wat SA 31:603–608

    Google Scholar 

  • Nyholm JR, Lundberg C, Andersson PL (2010) Biodegradation kinetics of selected brominated flame retardants in aerobic and anaerobic soil. Environ Pollut 158:2235–2240

    Article  CAS  Google Scholar 

  • Oleszkiewicz JA, Sharma VK (1990) Stimulation and inhibition of anaerobic processes by heavy metals: a review. Biol Wastes 31:45–67

    Article  CAS  Google Scholar 

  • Parawira W, Murto M, Read JS, Mattiasson B (2004) Volatile fatty acid production during anaerobic digestion of solid potato waste. J Chem Technol Biotechnol 79:673–677

    Article  CAS  Google Scholar 

  • Pardue JH, Kongara S, Jones WJ (1996) Effect of cadmium on reductive dechlorination of trichloroaniline. Environ Toxicol Chem 15:1083–1088

    Article  CAS  Google Scholar 

  • Patel VB, Patel AR, Patel MC, Madamwar DB (1993) Effect of metals on anaerobic digestion of water hyacinth-cattle dung. Appl Biochem Biotechnol 43:45–50

    Article  CAS  Google Scholar 

  • Pattra S, Sangyoka S, Boonmee M, Reungsang A (2008) Bio-hydrogen production from the fermentation of sugarcane bagasse hydrolysate by Clostridium butyricum. Int J Hydrogen Energy 33:5256–5265

    Article  CAS  Google Scholar 

  • Peng K, Li X, Luo C, Shen Z (2006) Vegetation composition and heavy metal uptake by wild plants at three contaminated sites in Xiangxi area; China. J Environ Sci Health Part A 40:65–76

    Google Scholar 

  • Pind PF, Angelidaki I, Ahring BK (2003) Dynamics of the anaerobic process: effects of volatile fatty acids. Biotechnol Bioeng 82:791–801

    Article  CAS  Google Scholar 

  • Raposo F, Banks CJ, Siegert I, Heaven S, Borja R (2006) Influence of inoculum to substrate ratio on the biochemical methane potential of maize in batch tests. Process Biochem 41:1444–1450

    Article  CAS  Google Scholar 

  • Roberts DJ, Venkataraman N, Pendharkar S (1998) The effect of metals on biological remediation of munitions contaminated soil. Environ Eng Sci 15:265–277

    Article  CAS  Google Scholar 

  • Sanchez E, Borja R, Weiland P, Travieso L, Martin A (2000) Effect of temperature and pH on the kinetics of methane production, organic nitrogen and phosphorus removal in the batch anaerobic digestion process of cattle manure. Bioprocess Biosys Eng 22:247–252

    Article  CAS  Google Scholar 

  • Sanchez E, Borja R, Travieso L, Martin A, Colmenarejo MF (2005) Effect of organic loading rate on the stability, operational parameters and performance of a secondary upflow anaerobic sludge bed reactor treating piggery waste. Bioresour Technol 96:335–344

    Article  CAS  Google Scholar 

  • Sandrin TR, Maier RM (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111:1093–1101

    Article  CAS  Google Scholar 

  • Schmidt JE, Ahring BK (1996) Granular sludge formation in upflow anaerobic sludge blanket UASB) reactors. Biotechnol Bioeng 49:229–246

    Article  CAS  Google Scholar 

  • Şengör SS, Barua S, Gikas P, Ginn TR, Peyton B, Sani RK, Spycher NF (2009) Influence of heavy metals on microbial growth kinetics including lag time: mathematical modeling and experimental verification. Environ Toxicol Chem 28:2020–2029

    Article  Google Scholar 

  • Siegert I, Banks C (2005) The effects of volatile fatty acid additions on the anaerobic digestion of cellulose and glucose in batch reactors. Process Biochem 40:3412–3418

    Article  CAS  Google Scholar 

  • Sondhi A, Guha S, Harendranath CS, Singh A (2010) Effect of aluminum (Al3+) on granulation in upflow anaerobic sludge blanket reactor treating low-strength synthetic wastewater. Wat Environ Res 82:715–724

    Article  CAS  Google Scholar 

  • Song YC, Kwon SJ, Woo JH (2004) Mesophilic and thermophilic temperature co-phase anaerobic digestion compared with single-stage mesophilic- and thermophilic digestion of sewage sludge. Wat Res 38:1653–1662

    Article  CAS  Google Scholar 

  • Tiwari MK, Guha S, Harendranath CS, Tripathi S (2006) Influence of extrinsic factors on granulation in UASB reactor. Appl Microbiol Biotechnol 71:145–154

    Article  CAS  Google Scholar 

  • Torkian A, Eqbali A, Hashemian SJ (2003) The effect of organic loading rate on the performance of UASB reactor treating slaughterhouse effluent. Resour Conserv Recycl 40:1–11

    Article  Google Scholar 

  • Uemura S, Harada H (1995) Inorganic composition and microbial characteristics of methanogenic granular sludge grown in a thermophilic upflow anaerobic sludge blanket reactor. Appl Microbiol Biotechnol 43:358–364

    Article  CAS  Google Scholar 

  • Veeken A, Kalyuzhnyi S, Scharff H, Hamelers B (2000) Effect of pH and VFA on hydrolysis of organic solid waste. J Environ Eng-ASCE 126:1076–1081

    Article  CAS  Google Scholar 

  • Velmurugan B, Ramanujam RA (2011) Anaerobic digestion of vegetable wastes for biogas production in a fed-batch reactor. Int J Emerging Sci 1:478–486

    Google Scholar 

  • Vlyssides A, Barampouti EM, Mai S (2009) Influence of ferrous iron on the granularity of a UASB reactor. Chem Eng J 146:49–56. http://dx.doi.org/10.1016/j.cej.2008.05.011

    Google Scholar 

  • Wang J, Wan W (2008) Influence of Ni2+ concentration on biohydrogen production. Bioresour Technol 99:8864–8868

    Article  CAS  Google Scholar 

  • Wang Y, Zhang Y, Wang J, Meng L (2009a) Effects of volatile fatty acids concentrations on methane yield and methanogenic bacteria. Biomass Bioenergy 33:848–853

    Article  CAS  Google Scholar 

  • Wang Y, Wu C, Wang X, Zhou S (2009b) The role of humic substances in the anaerobic reductive dechlorination of 2,4-dichlorophenoxyacetic acid by Comamonas koreensis strain CY01. J Hazard Mater 164:941–947

    Article  CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2012) Toxic effects of heavy metals on germination and physiological processes of plants. Toxic Heavy Met Legum Bioremediation 2:45–66

    Article  Google Scholar 

  • Weaver PF, Lien S, Seibert M (1980) Photobiological production of hydrogen. Sol Energy 24:3–45

    Article  CAS  Google Scholar 

  • Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85:849–860

    Article  CAS  Google Scholar 

  • Xue W, Wu C, Xiao K, Huang X, Zhou H, Tsuno H, Tanaka H (2010) Elimination and fate of selected micro-organic pollutants in a full-scale anaerobic/anoxic/aerobic process combined with membrane bioreactor for municipal wastewater reclamation. Wat Res 44:5999–6010

    Article  CAS  Google Scholar 

  • Yin F, Zhang WD, Liu SQ, Li JC, Xu R, Chen XB (2011) Discussing on biochemical pathway of anaerobic fermentation for hydrogen and methane production by Eupatorium Adenophorum Spreng based on biochemical materials. In: Zhang H, Jin D (eds) Advanced Research on Material Science, Environmental Science and Computer Science. Trans Tech Publications, Switzerland, pp 398–403

    Google Scholar 

  • Yoneyama Y, Nishii A, Nishimoto M, Yamada N, Suzuki T (2006) Upflow anaerobic sludge blanket (UASB) treatment of supernatant of cow manure by thermal pre-treatment. Wat Sci Technol 54:221–227

    Article  CAS  Google Scholar 

  • Yu HQ, Fang HHP (2001) Inhibition by chromium and cadmium of anaerobic acidogenesis. Wat Sci Technol 43:267–274

    CAS  Google Scholar 

  • Yu HQ, Mu Y (2006) Biological hydrogen production in a UASB reactor with granules. II: reactor performance in 3-year operation. Biotechnol Bioeng 94:988–995

    Article  CAS  Google Scholar 

  • Yu HQ, Fang HHP, Tay JH (2000) Effects of Fe2+ on sludge granulation in upflow anaerobic sludge blanket reactors. Wat Sci Technol 41:199–205

    CAS  Google Scholar 

  • Yue ZB; Yu HQ; Wang ZL (2007) Anaerobic digestion of cattail with rumen culture in the presence of heavy metals. Bioresour Technol 98:781–786. http://dx.doi.org/10.1016/j.biortech.2006.03.017

    Google Scholar 

  • Zayed G, Winter J (2000) Inhibition of methane production from whey by heavy metals-protective effect of sulfide. Appl Microbiol Biotechnol 53:726–731

    Article  CAS  Google Scholar 

  • Zhang YS; Zhang ZY; Suzuki K; Maekawa T (2003) Uptake and mass balance of trace metals for methane producing bacteria. Biomass Bioenergy 25:427–433. http://dx.doi.org/10.1016/S0961-9534(03)00012-6

    Google Scholar 

  • Zhang G-L, Yang F-G, Zhao Y-G, Zhao W-J, Yang J-L, Gong Z-T (2005) Historical change of heavy metals in urban soils of Nanjing; China during the past 20 centuries. Environ Int 31:913–919

    Article  CAS  Google Scholar 

  • Zhu H, Fang HHP, Zhang T, Beaudette LA (2007) Effect of ferrous ion on photo heterotrophic hydrogen production by Rhodobacter sphaeroides. Int J Hydrogen Energy 32:4112–4118. http://dx.doi.org/10.1016/j.ijhydene.2007.06.010

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Mudhoo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mudhoo, A., Kumar, S. Effects of heavy metals as stress factors on anaerobic digestion processes and biogas production from biomass. Int. J. Environ. Sci. Technol. 10, 1383–1398 (2013). https://doi.org/10.1007/s13762-012-0167-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13762-012-0167-y

Keywords

Navigation