Influence of Heavy Metals on the Process of Anaerobic Fermentation of Biomass by the Consortia of Anaerobic Microorganisms

Nataliia Golub, Andriy Shynkarchuk, Olexander Kozlovets, Shi Xinhua


Heavy metals released into the environment have a negative impact on the development of living organisms and soil fertility. The use of biomass obtained on such soils as a substrate for biogas production is problematic since heavy metals affect the consortia of microorganisms-decomposers and methane producers, and, consequently, the biogas yield. Therefore, the effect of certain metal ions and their concentrations in the environment on the development of the anaerobicconsortia for biogas production is the topical question. We are aimed to generalize research findings across the influence of heavy metal compounds on the process of anaerobic fermentation of biomass and determination of limiting concentrations for the functioning of the anaerobic consortia. Analysis of the literature has shown that the addition of heavy metal salts to the working medium affects the process of anaerobic fermentation, which depends on the form of the introduced metal, its concentration, the preliminary adaptation of the consortia to the metal. The biogas yield depends on the concentration of the element under study and the presence of other elements in the substrate. It has been established that the allow­able concentrations of metal ions are as follows: for іron – 20 g/l Fe0 or 500 mg/l K2FeO4; for chromium – 50 mg/l Cr3+; for copper – 40 mg/l CuCl2; for zinc – 40 mg/l ZnCl2. The data obtained on the influence of various concentrations of heavy metals on the anaerobic fermentation process will make it possible to model and conduct further studies of the effects of both individual heavy metal ions and their combinations on the biotechnology of processing waste containing such metals.


Heavy metals; Iron; Copper; Zinc; Chromium; Anaerobic microorganisms; Biogas


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. 2013;10:1383-98. DOI: 10.1007/s13762-012-0167-y

Zayed G, Winter J. Inhibition of methane production from whey by heavy metals - protective effect of sulfide. Appl Microbiol Biotechnol. 2000;53:726-31. DOI: 10.1007/s002530000336

Cirne DG, Paloumet X, Bjornsson L, Alves MM, Mattiasson B. Anaerobic digestion of lipid-rich waste: effects of lipid concentration. Renew Energy. 2007;32:965-75. DOI: 10.1016/j.renene.2006.04.003

Abou-Shanab RAI, Van Berkum P, Angle JS. Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere. 2007;68(2):360-7. DOI: 10.1016/j.chemosphere.2006.12.051

Tashirev AB, Romanovskaya VA, Rokitko PV, Tashireva AA. Multiple resistance to toxic metals of microorganisms in Antarctic cliffs (Galindez Island). Ukrainskyi Antarktychnyi Zhurnal. 2012;10-11:212-21. DOI: 10.33275/1727-7485.10-11.2012.301

Fashola M, Ngole-Jeme V, Babalola O. Heavy metal pollution from gold mines: environmental effects and bacterial strategies for resistance. Int J Environ Res Public Health. 2016;13(11):1047. DOI: 10.3390/ijerph13111047

Bertini I, Gray HB, Lippard SJ, Valentine J. Bioinorganic chemistry. Mill Valley: University Science Books; 1994. 611 p.

Tashirev AB. Interaction of microorganisms with metals. Mikrobiologichnyi Zhurnal. 1994;56(60):89-100.

Tashirev AB, Galinker EV, Andreyuk EI. Thermodynamic prediction of redox interaction of microorganisms with oxidizing metals (Hg2+, CrO42– and Cu2+). Reports of the National Academy of Sciences of Ukraine. 2008;4:166-72. Available from:

Gubsky YI. Biological chemistry. Kyiv, Ternopil: Ukrmedknyha; 2000. 507 p.

Topchiy NM. Influence of heavy metals on photosynthesis. Physiol Biochem Cult Plants. 2010;42(2):95-106.

Ianieva O. Mechanisms of bacteria resistance to heavy metals. Mikrobiologichnyi Zhurnal. 2009;71:54-65.

Dincă M, Moiceanu G, Paraschiv G, Voicu G, Ungureanu N, Toma L, et al. The influence of heavy metals on biogas production during the anaerobic digestion process. In: Proceedings of the 3rd International Conference on Thermal Equipment, Renewable Energy and Rural Development; 2014 June 12-14; Mamaia (Romania): University "Politehnica" of Bucharest.

Wu D, Zheng S, Ding A, Sun G, Yang M. Performance of a zero valent iron-based anaerobic system in swine wastewater treatment. J Hazard Mater. 2015;286:1-6. DOI: 10.1016/j.jhazmat.2014.12.029

Liu S, Yang G, Fu J, Zhang G. Synchronously enhancing biogas production, sludge reduction, biogas desulfurization, and digestate treatment in sludge anaerobic digestion by adding K2FeO4. Environ Sci Pollut Res Int. 2018;25:35154-63. DOI: 10.1007/s11356-018-3438-4

Feng Y, Zhang Y, Quan X, Chen S. Enhanced anaerobic digestion of waste activated sludge digestion by the addition of zero valent iron. Water Res. 2014;52:242-50. DOI: 10.1016/j.watres.2013.10.072

Liang YG, Li XJ, Zhang J, Zhang LG, Cheng B. Effect of microscale ZVI/magnetite on methane production and bioavailability of heavy metals during anaerobic digestion of diluted pig manure. Environ Sci Pollut Res Int. 2017;24(13):12328‐37. DOI: 10.1007/s11356-017-8832-9

Daddenavar KS, Manganure SA, Hiremath GM. Effect of elemental metals on methanogenesis by treating dairy wastewater. Int Res J Eng Technol. 2018;5(7):632-6.

Gonzalez-Silva BM, Briones-Gallardo R, Razo-Flores E, Celis LB. Inhibition of sulfate reduction by iron; cadmium and sulfide in granular sludge. J Hazard Mater. 2009;172:400-7. DOI: 10.1016/j.jhazmat.2009.07.022

Vlyssides A, Barampouti EM, Mai S. Influence of ferrous iron on the granularity of a UASB reactor. Chem Eng J. 2009;146:49-56. DOI: 10.1016/j.cej.2008.05.011

Jose MFS, Eric JS, Pedro JJA. Effect of Fe0 quantity on the efficiency of integrated microbial-Fe0 treatment processes. Chemosphere. 2004;54:823-9. DOI: 10.1016/j.chemosphere.2003.08.037

Abbas G, Khan MQ, Khan MJ, Hussain F, Hussain I. Effect of iron on the growth and yield contributing parameters of wheat (Triticum aestivum L.). J Animal Plant Sci. 2009;19(3):135-9.

Ananda N, Patil BN. Influence of zinc, iron and time of nitrogen application on growth, yield and quality of durum wheat. Karnataka J Agricult Sci. 2005;18(3):599-603.

Nataraja TH, Halepyati BK, Desaiand BT. Interactive effect of phosphorus, zinc, and iron on the productivity and nutrient uptake by durum wheat (Tritium durum Desf). Karnataka J Agricult Sci. 2005;18(4):907-10.

Garg SK, Tripathi M, Singh SK, Singh A. Pentachlorophenol dechlorination and simultaneous Cr6+ reduction by Pseudomonas putida SKG-1 MTCC (10510): characterization of PCP dechlorination products, bacterial structure, and functional groups. Environ Sci Pollut Res. 2013;20:2288-304. DOI: 10.1007/s11356-012-1101-z

Malaviya Р, Singh А. Bioremediation of chromium solutions and chromium containing wastewaters. Crit Rev Microbiol. 2016;42:607-33. DOI: 10.3109/1040841X.2014.974501

Oliveira H. Chromium as an environmental pollutant: Insights on induced plant toxicity. J Botany. 2012;12:375843. DOI: 10.1155/2012/375843

Barrera-Díaz CE, Lugo-Lugo V, Bilyeu B. A review of chemical, electrochemical and biological methods for aqueous Cr(VI) reduction. J Hazard Mater. 2012;223-224:1-12. DOI: 10.1016/j.jhazmat.2012.04.054

Joutey NT, Sayel H, Bahafid W, Ghachtouli NEl. Mechanisms of hexavalent chromium resistance and removal by microorganisms. Rev Environ Contam Toxicol. 2015;233:45-69. DOI: 10.1007/978-3-319-10479-9_2

Zhang S, Hao X, Tang J, Hu J, Deng Y, Xu M, et al. Assessing chromium contamination in red soil: monitoring the migration of fractions and the change of related microorganisms. Int J Environ Res Public Health. 2020;17(8):2835. DOI: 10.3390/ijerph17082835

Viti C, Marchi E, Decorosi F, Giovannetti L. Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol Rev. 2014;38(4):633-59. DOI: 10.1111/1574-6976.12051

Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H, Torres-Guzmán JC, et al. Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev. 2001;25(3):335-47. DOI: 10.1111/j.1574-6976.2001.tb00581.x

Ramírez-Díaz MI, Díaz-Pérez C, Vargas E, Riveros-Rosas H, Campos-García J, Cervantes C. Mechanisms of bacterial resistance to chromium compounds. Biometals. 2008;21(3):321-32. DOI: 10.1007/s10534-007-9121-8

Pakholkiv NI, Luchka IV, Dzen EO, Kurtyak BM, Chornoshkin BO. Influence of organic and inorganic forms of chromium on cellulosolytic and amylolytic activity of cattle rumen microorganisms. Foothill and Mountain Agriculture and Stockbreeding. 2013;55(1):165-9.

Cheung KH, Gu JD. Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeter Biodegrad. 2007;59:8-15. DOI: 10.1016/j.ibiod.2006.05.002

Andreyuk EI, Tashirev AB, Smalko PY. Prediction of the interaction of microorganisms with chromium compounds based on thermodynamic calculations. Reports of the National Academy of Sciences of Ukraine. 2003;1:149-56.

Prasad PVVV, Das C, Golder AK. Reduction of Cr(VI) to Cr(III) and removal of total chromium from wastewater using scrap iron in the form of zerovalent iron(ZVI): Batch and column studies. Canadian J Chem Eng. 2011;89(6):1575-82. DOI: 10.1002/cjce.20590

Kanagaraj J, Velappan KC, Chandra Babu NK, Sadulla S. Solid wastes generation in the leather industry and its utilization for cleaner environment - a review. J Sci Ind Res. 2006;65:541-8. DOI: 10.1002/chin.200649273

Mandan B, Fathima NN, Rao JR, Nair BU. New chromium-zinc tanning agent: A viable option for less chrome technology. J Am Leather Chem Assoc. 2002;97:189-96.

Dhayalan K, Fathima NN, Gnanamani A, Rao JR, Nair BU, Ramasami T. Biodegradability of leathers through anaerobic pathway. Waste Manag. 2006;27(6):760-7. DOI: 10.1016/j.wasman.2006.03.019

Pessuto J, Godinho M, Dettmer A. Biogas production from tannery wastes. Evaluation of isolated microorganisms effect. In: Proceedings of XXXIII IULTCS Congress; 2015 November 24-27; Novo Hamburgo (Brazil): ABQTIC.

Quang LH. Making use of tannery chromium containing sludge as feed for biogas plant [bachelor thesis]. Kokkola: Central Ostrobothnia University of Applied; 2011. 67 p.

Deublein D, Steinhauser A. Biogas from waste and renewable resources: an introduction. Weinheim: Wiley-VCH; 2008. 578 p. DOI: 10.1002/9783527632794

Suresh G, Ravichandran N, Ramesh B, Suresh A, Siva GV. Isolation and characterization of chromium-tolerant bacteria from chromium-containing waste water. Bioremed Biodiver Bioavail. 2011;5(1):22-7.

Das AP, Mishra S. Biodegradation of the metallic carcinogen hexavalent chromium Cr(VI) by an indigenously isolated bacterial strain. J Carcinog. 2010;9:1-6. DOI: 10.4103/1477-3163.63584

Mishra S, Doble M. Novel chromium tolerant microorganisms: isolation, characterization and their biosorption capacity. Ecotoxicol Environ Safe. 2008;71:874-9. DOI: 10.1016/j.ecoenv.2007.12.017

Ge S, Zhou M, Dong X, Lu Y, Ge S. Distinct and effective biotransformation of hexavalent chromium by a novel isolate under aerobic growth followed by facultative anaerobic incubation. Appl Microbiol Biotechnol. 2013;97:2131-7. DOI: 10.1007/s00253-012-4361-0

Rensing C, Grass G. Escherichia coli mechanisms of copperhomeostasis in a changing environment. FEMS Microbiol Rev. 2003;27:197-213. DOI: 10.1016/S0168-6445(03)00049-4

Dupont CL, Grass G, Rensing C. Copper toxicity and the origin of bacterial resistance - New insights and applications. Metallomics. 2011;3:1109-18. DOI: 10.1039/c1mt00107h

Samanovic MI, Ding C, Thiele DJ, Darwin KH. Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe. 2012;11(2):106-15. DOI: 10.1016/j.chom.2012.01.009

Palmgren MG, Nissen P. Review P-type ATPases. Annu Rev Biophys. 2011;40:243-66. DOI: 10.1146/annurev.biophys.093008.131331

Festa RA, Jones MB, Butler-Wu S, Sinsimer D, Gerads R, Bishai WR, et al. A novel copper-responsive regulon in Mycobacterium tuberculosis. Mol Microbiol. 2011;79:133-48. DOI: 10.1111/j.1365-2958.2010.07431.x

Ladomersky E, Petris MJ. Copper tolerance and virulence in bacteria. Metallomics. 2015;7(6):957-64. DOI: 10.1039/c4mt00327f

Kushkevich I, Hnatush S, Hudz S. Influence of heavy metals on cells of microorganisms. Bulletin of Lviv University. 2007;45:3-28. Available from:

Jungin OS, Belikova EY, Gladka GV, Tashirev AB. Genetic potential of bacteria isolated from cadmium contaminated soils. Faktory Eksperymentalʹnoyi Evolyutsiyi Orhanizmiv. 2018;23:352-6.

Zayed G, Winter J. Inhibition of methane production from whey by heavy metals - protective effect of sulfide. Appl Microbiol Biotechnol. 2000;53:726-31. DOI: 10.1007/s002530000336

Mertens J, Degryse F, Springael D, Smolders E. Zinc toxicity to nitrification in soil and soilless culture can be predicted with the same biotic ligand model. Environ Sci Technol. 2007;41:2992-7. DOI: 10.1021/es061995+

Abdel AA., Rittmann SKR., Fino D, Bochmann G. The physiological effect of heavy metals and volatile fatty acids on Methanococcus maripaludis S2. Biotechnol Biofuels. 2018;11:301. DOI: 10.1186/s13068-018-1302-x

Dopson M, Baker-Austin C, Koppineedi P, Bond PL. Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic microorganisms. Microbiology. 2003;149:1959-70. DOI: 10.1099/mic.0.26296-0

Takashima M, Shimada K, Speece RE. Minimum requirements for trace metals (Iron, Nickel, Cobalt, and Zinc) in thermophilic and mesophilic methane fermentation from glucose. Water Environ Res. 2011;83(4):339-46. DOI: 10.2175/106143010x12780288628895

Chen M, Cui Y, Bai F, Wang J. Effect of two biogas residues' application on copper and zinc fractionation and release in different soils. J Environ Sci. 2013;25(9):1865-73. DOI: 10.1016/s1001-0742(12)60246-0

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