World Journal of Microbiology and Biotechnology

, Volume 31, Issue 10, pp 1501–1515 | Cite as

Biological technologies for the removal of sulfur containing compounds from waste streams: bioreactors and microbial characteristics

  • Lin LiEmail author
  • Jingying Zhang
  • Jian Lin
  • Junxin Liu


Waste gases containing sulfur compounds, such as hydrogen sulfide, sulfur dioxide, thioethers, and mercaptan, produced and emitted from industrial processes, wastewater treatment, and landfill waste may cause undesirable issues in adjacent areas and contribute to atmospheric pollution. Their control has been an area of concern and research for many years. As alternative to conventional physicochemical air pollution control technologies, biological treatment processes which can transform sulfur compounds to harmless products by microbial activity, have gained in popularity due to their efficiency, cost-effectiveness and environmental acceptability. This paper provides an overview of the current biological techniques used for the treatment of air streams contaminated with sulfur compounds as well as the advances made in the past year. The discussion focuses on bioreactor configuration and design, mechanism of operation, insights into the overall biological treatment process, and the characterization of the microbial species present in bioreactors, their populations and their interactions with the environment. Some bioreactor case studies are also introduced. Finally, the perspectives on future research and development needs in this research area were also highlighted.


Air pollution control Bioreactors Sulfur containing compounds Microbial characterization Desulfurization bacteria 



The authors express their sincere thanks to Dr. Watts for the English revision of the manuscript. This work was financially supported by the Major Science and Technology Program for Water Pollution Control and Treatment (No. 2010ZX07319-001-03) and the National Natural Science Foundation of China (No. 51478456).


  1. An TC, Wan SG, Li GY, Sun L, Guo B (2010) Comparison of the removal of ethanethiol in twin-biotrickling filters inoculated with strain RG-1 and B350 mixed microorganisms. J Hazard Mater 183:372–380CrossRefGoogle Scholar
  2. Anet B, Lemasle M, Couriol C, Lendormi T, Amrane A, Cloirec PL, Cogny G, Fillières R (2013) Characterization of gaseous odorous emissions from a rendering plant by GC/MS and treatment by biofiltration. J Environ Manag 128:981–987CrossRefGoogle Scholar
  3. Asano R, Hirooka K, Nakai Y (2012) Middle-thermophilic sulfur-oxidizing bacteria Thiomonas sp. RAN5 strain for hydrogen sulfide removal. J Air Waste Manag Assoc 62:38–43CrossRefGoogle Scholar
  4. Atanes E, Nieto-Marquez A, Cambra A, Ruiz-Perez MC, Fernandez-Martinez F (2012) Adsorption of SO2 onto waste cork powder-derived activated carbons. Chem Eng J 211:60–67CrossRefGoogle Scholar
  5. Baspinara AB, Turkera M, Hocalara A, Ozturkb I (2011) Biogas desulphurization at technical scale by lithotrophicdenitrification: integration of sulphide and nitrogen removal. Process Biochem 46:916–922CrossRefGoogle Scholar
  6. Braun-Lüllemann A, Majcherczyk A, Hüttermann A (1997) Biodegradation of styrene by white-rot fungi. Appl Microbiol Biotechnol 47:150–155CrossRefGoogle Scholar
  7. Cha JM, Cha WS, Lee J (1999) Removal of organo-sulphurodour compounds by Thiobacillusnovellus SRM, sulphur-oxidizing microorganisms. Process Biochem 34:659–665CrossRefGoogle Scholar
  8. Chen YQ, Fan ZD, Ma LX, Yin J, Luo M, Cai WF (2014) Performance of three pilot-scale immobilized-cell biotrickling filters for removal of hydrogen sulfide from a contaminated air steam. Saudi J Biol Sci 21:450–456CrossRefGoogle Scholar
  9. Cho KS, Hirai M, Shoda M (1991) Degradation characteristics of hydrogen sulfide, methanethiol, dimethyl sulfide and dimethyl disulfide by Thiobacillus thioparus DW44 isolated from peat biofilter. J Ferment Bioeng 71:384–389CrossRefGoogle Scholar
  10. Chung YC, Huang C, Tseng CP (1996) Biodegradation of hydrogen sulfide by a laboratory-scale immobilized pseudomonas putida CH11 biofilter. Biotechnol Progr 12:773–778CrossRefGoogle Scholar
  11. Cox HHJ, Deshusses MA (2002) Co-treatment of H2S and toluene in a biotrickling filter. Chem Eng J 87:101–110CrossRefGoogle Scholar
  12. De Bo I, Van Langenhove H, Heyman J, Vincke J, Verstraete W, Van Langenhove H (2003) Dimethyl sulfide removal from synthetic waste gas using a flat poly(dimethylsiloxane)-coated composite membrane bioreactor. Enviorn Sci Technol 37:4228–4234CrossRefGoogle Scholar
  13. Degorce-Dumas JR, Kowal S, Le Cloirec P (1997) Microbiological oxidation of hydrogen sulphide in a biofilter. Can J Microbiol 43:264–271CrossRefGoogle Scholar
  14. Delhomenie MC, Heitz M (2005) Biofiltration of air: a review. Crit Rev Biotechnol 25:53–72CrossRefGoogle Scholar
  15. Deshusses MA (1997) Biological waste air treatment in biofilters. Curr Opin Biotechnol 3:335–339CrossRefGoogle Scholar
  16. Devinny JS, Deshusses MA, Webster TS (1999) Biofiltration for air pollution control. Lewis Publ, New York, pp 43, 78Google Scholar
  17. Durme JV, Dewulf J, Leys C, Langenhove HV (2008) Combining non-thermal plasma with heterogeneous catalysis in waste gas treatment: a review. Appl Catal B Envion 78:324–333CrossRefGoogle Scholar
  18. Elmi F, Etemadifar Z, Emtiazi G (2015) A novel metabolite (1,3-benzenediol, 5-hexyl) production by Exophialaspinifera strain FM through dibenzothiophene desulfurization. World J Microbiol Biotechnol 31:813–821CrossRefGoogle Scholar
  19. Estrada JM, Kraakman NJR, Lebrero R, Muñoz R (2012) A sensitivity analysis of process design parameters, commodity prices and robustness on the economics of odour abatement technologies. Biotechnol Adv 30:1354–1363CrossRefGoogle Scholar
  20. Fortuny M, Gamisans X, Deshusses MA, Lafuente J, Casas C, Gabriel D (2011) Operational aspects of the desulfurization process of energy gases mimics in biotrickling filters. Water Res 45:5665–5674CrossRefGoogle Scholar
  21. Furusawa N, Togashi I, Hirai M, Kubota H (1984) Removal of hydrogen sulfide by a biofilter with fibrous peat. J Ferment Technol 62:589–594Google Scholar
  22. Gao M, Li L, Liu JX (2011) Simultaneous removal of hydrogen sulfide and toluene in a bioreactor: performance and characteristics of microbial community. J Environ Sci 23:353–359CrossRefGoogle Scholar
  23. Gilbert ES, Walker AW, Keasling JD (2003) A constructed microbial consortium for biodegradation of the organophosphorus insecticide parathion. Appl Microbiol Biotechnol 61:77–81CrossRefGoogle Scholar
  24. Giri BS, Pandey RA (2013) Biological treatment of gaseous emissions containing dimethyl sulphide generated from pulp and paper industry. Bioresour Technol 142:420–427CrossRefGoogle Scholar
  25. Giri BS, Mudliar SN, Deshmukh SC, Banerjee S, Pandey RA (2010) Treatment of waste gas containing low concentration of dimethyl sulphide (DMS) in a bench-scale biofilter. Bioresour Technol 101:2185–2190CrossRefGoogle Scholar
  26. González-Sánchez A, Revah S, Deshusses MA (2008) Alkaline biofiltration of H2S odors. Environ Sci Technol 42(19):7398–7404CrossRefGoogle Scholar
  27. Hirano T, Kurosawa H, Nakamura K, Amano Y (1996) Simultaneous removal of hydrogen sulfide and trimethylamine by a bacterial deodorant. J Ferment Bioeng 81:337–342CrossRefGoogle Scholar
  28. Ho KL, Chung YC, Lin YH, Tseng CP (2008) Microbial populations analysis and field application of biofilter for the removal of volatile-sulfur compounds from swine wastewater treatment system. J Hazard Mater 152:580–588CrossRefGoogle Scholar
  29. Honma T, Akino T (1998) Isolation and characterization of a hydrogen sulfide-removing bacterium, Pseudomonas sp. strain DO-1. Biosci Biotechnol Biochem 62:1684–1687CrossRefGoogle Scholar
  30. Hort C, Gracy S, Platel V, Moynault L (2009) Evaluation of sewage sludge and yard waste compost as a biofilter media for the removal of ammonia and volatile organic sulfur compounds (VOSCs). Chem Eng J 152:44–53CrossRefGoogle Scholar
  31. Ishikawa H, Kita Y, Horikoshi K (1980) United States Patent, 4, 225, 381Google Scholar
  32. Ito T, Miyaji T, Nakagawa T, Tomizuka N (2007) Degradation of dimethyl disulfide by Pseudomonas fluorescens strain 76. Biosci Biotechnol Biochem 71:366–370CrossRefGoogle Scholar
  33. Itoh N, Yoshida M, Miyamoto T, Ichinose H, Wariishi H, Tanaka H (1997) Fungal cleavage of thioether bond found in Yperite. FEBS Lett 412:281–284CrossRefGoogle Scholar
  34. Jaber MB, Anet B, Amrane A, Couriol C, Lendormi T, Cloirec PL, Cogny G, Fillières R (2014) Impact of nutrients supply and pH changes on the elimination of hydrogen sulfide, dimethyl disulfide and ethanethiol by biofiltration. Chem Eng J 258:420–426CrossRefGoogle Scholar
  35. Kennes C, Veiga MC (2004) Fungal biocatalysts in the biofiltration of VOC-polluted air. J Biotechnol 113:305–319CrossRefGoogle Scholar
  36. Kong Z, Farhana L, Fulthorpe RR, Allen DG (2001) Treatment of volatile organic compounds in a biotrickling filter under thermophilic conditions. Environ Sci Technol 35:4347–4352CrossRefGoogle Scholar
  37. Kumar A, Chilongo T, Dewulf J, Ergas SJ, Van Langenhove H (2010) Gaseous dimethyl sulphide removal in a membrane biofilm reactor: effect of methanol on reactor performance. Bioresour Technol 101:8955–8959CrossRefGoogle Scholar
  38. Lebrero R, Rodríguez E, Martin M, García-Encina PA, Muñoz R (2010) H2S and VOCs abatement robustness in biofilters and air diffusion bioreactors: a comparative study. Water Res 44:3905–3914CrossRefGoogle Scholar
  39. Li L, Liu JX (2004) Study on odors treatment by the combination o f bacteria and fungi. Environ Sci 25:22–26 (in Chinese) Google Scholar
  40. Li L, Liu JX (2006) Removal of xylene from off-gas using a bioreactor containing bacteria and fungi. Int Biodeter Biodegr 58:60–64CrossRefGoogle Scholar
  41. Li L, Liu JX (2009) Identification and characteristic analysis of microorganisms in an integrated bioreactor for odours treatment. Int J Environ Pollut 37:216–234CrossRefGoogle Scholar
  42. Li L, Wang SB, Feng QC, Liu JX (2008a) Removal of o-xylene from off-gas by a combination of bioreactor and adsorption. Asia-Pac J Chem Eng 3:489–496CrossRefGoogle Scholar
  43. Li L, Yang C, Lan WS, Xie S, Qiao CL, Liu JX (2008b) Removal of methyl parathion from artificial off-gas using a bioreactor containing a constructed microbial consortium. Environ Sci Technol 42:2136–2141CrossRefGoogle Scholar
  44. Li L, Liu SQ, Liu JX (2011a) Surface modification of coconut shell based activated carbon for the improvement of hydrophobic VOC removal. J Hazard Mater 192:683–690CrossRefGoogle Scholar
  45. Li L, Yang C, He YQ, Qiao CL, Liu JX (2011b) Simultaneous removal of parathion and methyl parathion by genetically engineered Escherichia coli in a biofilter treating polluted air. Int J Environ Pollut 45:3–14CrossRefGoogle Scholar
  46. Li L, Lian J, Han YP, Liu JX (2012) A biofilter integrated with gas membrane separation unit for the treatment of fluctuating styrene loads. Bioresour Technol 111:76–83CrossRefGoogle Scholar
  47. Li L, Han YP, Yan X, Liu JX (2013) H2S removal and bacterial structure along a full-scale biofilter bed packed with polyurethane foam in a landfill site. Bioresour Technol 147:52–58CrossRefGoogle Scholar
  48. Li GY, Liang ZS, An TC, Zhang ZY, Chen XQ (2015a) Efficient bio-deodorization of thioanisole by a novel bacterium Brevibacillusborstelensis GIGAN1 immobilized onto different parking materials in twin biotrickling filter. Bioresour Technol 182:82–88CrossRefGoogle Scholar
  49. Li L, Zhang MZ, Liu JX (2015b) An integrated equipment and method for coprocessing of methane and malodorous substances. ZL201210238668.0Google Scholar
  50. Liang WJ, Fang HP, Li J, Zheng F, Li JX, Jin YQ (2011) Performance of nonthermal DBD plasma reactor during the removal of hydrogen sulfide. J Electrost 69:206–213CrossRefGoogle Scholar
  51. Liu JW, Liu JX, Li L (2008) Performance of two biofilters with neutral and low pH treating off-gases. J Environ Sci 20:1409–1414CrossRefGoogle Scholar
  52. Luvsanjamba M, Kumar A, Van Langenhove H (2008) Removal of dimethyl sulfide in a thermophilic membrane bioreactor. J Chem Technol Biotechnol 83:1218–1225CrossRefGoogle Scholar
  53. Moe WM, Qi B (2004) Performance of a fungal biofilter treating gas-phase solvent mixtures during intermittent loading. Water Res 38:2259–2268CrossRefGoogle Scholar
  54. Mohammad BT, Veiga MC, Kennes C (2007) Mesophilic and thermophilic biotreatment of BTEX-polluted air in reactors. Biotechnol Bioeng 97:1423–1438CrossRefGoogle Scholar
  55. Montebello AM, Fernández M, Almenglo F, Ramírez M, Cantero D, Baeza M, Gabriel D (2012) Simultaneous methylmercaptan and hydrogen sulfide removal in the desulfurization of biogas in aerobic and anoxic biotrickling filters. Chem Eng J 200–202:237–246CrossRefGoogle Scholar
  56. Morales M, Silva J, Morales P, Gentina JC, Aroca G (2012) Biofiltration of hydrogen sulfide by Sulfolobusmetallicus at high temperatures. Water Sci Technol 66:1958–1961CrossRefGoogle Scholar
  57. Moriarty DJ, Nicholas DJ (1970) Products of sulphide oxidation in extracts of Thiobacillusconcretivorus. Biochim Biophys Acta 197:143–151CrossRefGoogle Scholar
  58. Omri I, Bouallagui H, Aouidi F, Godo J-J, Hamdi M (2011) H2S gas biological removal efficiency and bacterial community diversity in biofilters treating wastewater odor. Bioresour Technol 102:10202–10209CrossRefGoogle Scholar
  59. Ottengraf SPP, Meesters JJP, Van Den Oever AHC, Rozema HR (1986) Biological elimination of volatile xenobiotic compounds in biofilters. Bioprocess Eng 1:61–69CrossRefGoogle Scholar
  60. Park SJ, Hirai M, Shoda M (1993) Treatment of exhaust gases from a night soil treatment plant by a combined deodorization system of activated carbon fabric reactor and peat biofilter inoculated with Thiobacillusthioparus DW44. J Ferment Bioeng 76:423–426CrossRefGoogle Scholar
  61. Phae C-G, Shoda M (1991) A new fungus which degrades hydrogen sulfide, methanethiol, dimethyl sulfide and dimethyl disulfide. Biotechnol Lett 13:375–380CrossRefGoogle Scholar
  62. Philip L, Deshusses MA (2003) Sulfur dioxide treatment from flue gases using a biotrickling filter-bioreactor system. Environ Sci Technol 37:1978–1982CrossRefGoogle Scholar
  63. Potivichayanon S, Pokethitiyook P, Kruatrachue M (2006) Hydrogen sulfide removal by a novel fixed-film bioscrubber system. Process Biochem 41:708–715CrossRefGoogle Scholar
  64. Ralebitso-Senior TK, Senior E, Di Felice R, Jarvis K (2012) Waste gas biofiltration: advances and limitations of current approaches in microbiology. Environ Sci Technol 46:8542–8573CrossRefGoogle Scholar
  65. Ramírez M, Fernández M, Granada C, Le Borgne S, Gómez JM, Cantero D (2011) Biofiltration of reduced sulphur compounds and community analysis of sulphur-oxidizing bacteria. Bioresour Technol 102:4047–4053CrossRefGoogle Scholar
  66. Rattanapan C, Kantachote D, Yan R, Boonsawang P (2010) Hydrogen sulfide removal using granular activated carbon biofiltration inoculated with Alcaligenesfaecalis T307 isolated from concentrated latex wastewater. Int Biodeter Biodegr 64:383–387CrossRefGoogle Scholar
  67. Reij MW, Keurentjes JTF, Hartmas S (1998) Membrane bioreactors for waste gas treatment. J Biotechnol 59:155–167CrossRefGoogle Scholar
  68. Ryu HW, Yoo SK, Choi JM, Cho KS, Cha DK (2009) Thermophilic biofiltration of H2S and isolation of a thermophilic and heterotrophic H2S-degrading bacterium, Bacillus sp. TSO3. J Hazard Mater 168:501–506CrossRefGoogle Scholar
  69. Sercu B, Núñez D, Aroca G, Boon N, Verstraete W, Van Langenhove H (2005) Inoculation and start-up of a biotricking filter removing dimethyl sulfide. Chem Eng J 113:127–134CrossRefGoogle Scholar
  70. Shanchayan B, Parker W, Pride C (2006) Dynamic analysis of a biofilter treating autothermal thermophilic aerobic digestion offgas. J Environ Eng Sci 5:263–272CrossRefGoogle Scholar
  71. Shu C-H, Chen C-K (2009) Enhanced removal of dimethyl sulfide from a synthetic waste gas stream using a bioreactor inoculated with Microbacterium sp. NTUT26 and Pseudomonas putida. J Ind Microbiol Biotechnol 36:95–104CrossRefGoogle Scholar
  72. Smith SJ, Pitcher H, Wigley TML (2001) Global and regional anthropogenic sulfur dioxide emissions. Global Planet Change 29:99–119CrossRefGoogle Scholar
  73. Solcia RB, Ramíreza M, Fernández M, Cantero D, Bevilaqu D (2014) Hydrogen sulphide removal from air by biotrickling filter using open-pore polyurethane foam as a carrier. Biochem Eng J 84:1–8CrossRefGoogle Scholar
  74. Tosati J, Jinsiriwanit S (2013) Improving the quality of hydrogen sulfide contaminated biogas by bioscrubber. Cur Opin Biotechnol 24:48–143CrossRefGoogle Scholar
  75. Van Groenestijn JW, Hesselink PGM (1993) Biotechniques for air pollution control. Biodegradation 4:283–301CrossRefGoogle Scholar
  76. Van Groenestijn JW, Liu JX (2002) Removal of alpha-pinene from gases using biofilters containing fungi. Atmos Environ 36:5501–5508CrossRefGoogle Scholar
  77. Volckaert D, Wuytens S, Van Langenhove H (2014) Two phase partitioning membrane bioreactor: a novel biotechnique for the removal of dimethyl sulphide, n-hexane and toluene from waste air. Chem Eng J 256:160–168CrossRefGoogle Scholar
  78. Weber FJ, Hartmans S (1992) Biological waste gas treatment with integrated adsorption for the treatment of fluctuating concentrations. In: Dragt AJ, van Ham J (eds) Biotechniques for air pollution abatement and odour control policies, proceedings of an international symposium, Maastricht, The Netherlands, pp 27–29Google Scholar
  79. Wei ZS, Li HQ, He JC, Ye QH, Huang QR, Luo YW (2013) Removal of dimethyl sulfide by the combination of non-thermal plasma and biological process. Bioresour Technol 146:451–456CrossRefGoogle Scholar
  80. Yang Y, Allen ER (1994) Biofiltration control of hydrogen sulfide1: design and operational parameters. J Air Waste Manage Assoc 44:863–868CrossRefGoogle Scholar
  81. Yang C, Liu N, Guo X, Qiao C (2006) Cloning of mpd gene from a chlorpyrifos-degrading bacterium and use of this strain in bioremediation of contaminated soil. FEMS Microbiol Lett 265:118–125CrossRefGoogle Scholar
  82. Zhang JY, Li L, Liu JX (2015) Thermophilic biofilter for SO2 removal: performance and microbial characteristics. Bioresour Technol 180:106–111CrossRefGoogle Scholar
  83. Zhu GY, Liu JX (2004) Investigation of factors on a fungal biofilter to treat waste gas with ethyl mercaptan. J Environ Sci 16:898–900Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Research Center for Eco-Environmental SciencesChinese Academy of SciencesBeijingChina

Personalised recommendations