Reviewing microbial electrical systems and bacteriophage biocontrol as targeted novel treatments for reducing hydrogen sulfide emissions in urban sewer systems

  • Elizabeth R. Mathews
  • Dean Barnett
  • Steve Petrovski
  • Ashley E. FranksEmail author
Review Paper


Microbially induced concrete corrosion (MICC) is a costly, and ongoing problem affecting the infrastructure of water utilities worldwide. Traditionally MICC has been treated with chemicals and physical techniques that inhibit the release of hydrogen sulfide (H2S), preventing sulfuric acid formation and the consequent corrosion. However, these methods require continual dosing and monitoring to ensure process efficiency and prevent undue costs. This review focuses on recent research into two potential novel treatments for MICC: re-engineering the sewer sulfur cycle by removing sulfide using electrodes in microbial electrical systems as an alternative electron acceptor and; altering the microbial community using targeted bacteriophage biocontrol to reduce specific sulfide-producing bacteria. These novel treatments hold the potential to reduce water utilities reliance on continual chemical dosing providing a long-lasting treatment I believe necessitates further laboratory and field-trial investigation.


Sewer corrosion Microbially induced concrete corrosion Microbial fuel cell Bacteriophage biocontrol Hydrogen sulfide Sulfate-reducing bacteria 



Acidophilic sulfur-oxidising bacteria


Electrochemically active microorganism


Free nitrous acid


Hydrogen sulfide


Microbial electrical systems


Microbial fuel cell


Microbially induced concrete corrosion


Sulfur-oxidising bacteria


Sulfide-producing bacteria


Sulfate-reducing bacteria



The author ERM, acknowledges the financial support of an Australian Postgraduate Award at La Trobe University and additional financial support from industry collaborators Western Water.


  1. Aminov RI (2010) A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 1:1–7. CrossRefGoogle Scholar
  2. Anderson RT, Vrionis HA, Ortiz-Bernad I et al (2003) Stimulating the in situ activity of geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl Environ Microbiol 69:5884–5891. CrossRefGoogle Scholar
  3. Bergel A, Féron D, Mollica A (2005) Catalysis of oxygen reduction in PEM fuel cell by seawater biofilm. Electrochem Commun 7:900–904. CrossRefGoogle Scholar
  4. Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485. CrossRefGoogle Scholar
  5. Bradley AS, Leavitt WD, Johnston DT (2011) Revisiting the dissimilatory sulfate reduction pathway. Geobiology 9:446–457. CrossRefGoogle Scholar
  6. Butti SK, Velvizhi G, Sulonen MLK et al (2016) Microbial electrochemical technologies with the perspective of harnessing bioenergy: maneuvering towards upscaling. Renew Sustain Energy Rev 53:462–476. CrossRefGoogle Scholar
  7. Cai J, Zheng P, Qaisar M, Sun P (2014) Effect of electrode types on simultaneous anaerobic sulfide and nitrate removal in microbial fuel cell. Sep Purif Technol 134:20–25. CrossRefGoogle Scholar
  8. Candena F, Peters RW (1988) Evaluation of chemical oxidizers for hydrogen sulfide control. J Water Pollut Control Fed 60:1259–1263Google Scholar
  9. Chambers LA, Trudinger PA (1975) Are thiosulfate and trithionate intermediates in dissimilatory sulfate reduction? J Bacteriol 123:36–40Google Scholar
  10. Cheng S, Logan BE (2007) Ammonia treatment of carbon cloth anodes to enhance power generation of microbial fuel cells. Electrochem Commun 9:492–496. CrossRefGoogle Scholar
  11. Chou TY, Whiteley CG, Lee DJ, Liao Q (2013) Control of dual-chambered microbial fuel cell by anodic potential: implications with sulfate reducing bacteria. Int J Hydrogen Energy 38:15580–15589. CrossRefGoogle Scholar
  12. Chou TY, Whiteley CG, Lee DJ (2014) Anodic potential on dual-chambered microbial fuel cell with sulphate reducing bacteria biofilm. Int J Hydrogen Energy 39:19225–19231. CrossRefGoogle Scholar
  13. Couvert A, Charron I, Laplanche A et al (2006) Treatment of odorous sulphur compounds by chemical scrubbing with hydrogen peroxide—stabilisation of the scrubbing solution. Chem Eng Sci 61:7240–7248. CrossRefGoogle Scholar
  14. Dumas C, Mollica A, Féron D et al (2007) Marine microbial fuel cell: use of stainless steel electrodes as anode and cathode materials. Electrochim Acta 53:468–473. CrossRefGoogle Scholar
  15. Dutta PK, Rozendal RA, Yuan Z et al (2009) Electrochemical regeneration of sulfur loaded electrodes. Electrochem Commun 11:1437–1440. CrossRefGoogle Scholar
  16. Eaktasang N, Min H-S, Kang C, Kim HS (2013) Control of malodorous hydrogen sulfide compounds using microbial fuel cell. Bioprocess Biosyst Eng 36:1417–1425. CrossRefGoogle Scholar
  17. Fan Y, Xu S, Schaller R et al (2011) Biosensors and Bioelectronics Nanoparticle decorated anodes for enhanced current generation in microbial electrochemical cells. Biosens Bioelectron 26:1908–1912. CrossRefGoogle Scholar
  18. Firer D, Friedler E, Lahav O (2008) Control of sulfide in sewer systems by dosage of iron salts: comparison between theoretical and experimental results, and practical implications. Sci Total Environ 392:145–156. CrossRefGoogle Scholar
  19. Frechen F-B, Romaker J, Giebel SM (2014) Controlling chemical dosing into sewers for odour and corrosion abatement. Chem Eng Trans 40:217–222. CrossRefGoogle Scholar
  20. Ganigué R, Jiang G, Sharma K et al (2016) Online Control of magnesium hydroxide dosing for sulfide mitigation in sewers: algorithm development, simulation analysis, and field validation. J Environ Eng 142:04016069 1–04016069 9. CrossRefGoogle Scholar
  21. Ge H, Zhang L, Batstone DJ et al (2013) Impact of Iron salt dosage to sewers on downstream anaerobic sludge digesters: sulfide control and methane production. J Environ Eng 139:594–601. CrossRefGoogle Scholar
  22. Goldnik E, Turek T (2016) Removal of hydrogen sulfide by permanganate based sorbents: experimental investigation and reactor modeling. Chem Eng Sci 151:51–63. CrossRefGoogle Scholar
  23. Gomez-Alvarez V, Revetta RP, Domingo JWS (2012) Metagenome analyses of corroded concrete wastewater pipe biofilms reveal a complex microbial system. BMC Microbiol 12:2–14. CrossRefGoogle Scholar
  24. Gong C, Jiang X (2015) Application of bacteriophages to reduce biofilms formed by hydrogen sulfide producing bacteria on surfaces in a rendering plant. Can J Microbiol 61:539–544. CrossRefGoogle Scholar
  25. Gong C, Heringa S, Singh R et al (2013) Isolation and characterization of bacteriophages specific to hydrogen-sulfide-producing bacteria. Can J Microbiol 59:39–45. CrossRefGoogle Scholar
  26. Gong C, Liu X, Jiang X (2014) Application of bacteriophages specific to hydrogen sulfide-producing bacteria in raw poultry by-products. Poult Sci 93:702–710. CrossRefGoogle Scholar
  27. Gregory KB, Lovley DR (2005) Remediation and recovery of uranium from contaminated subsurface environments with electrodes. Environ Sci Technol 39:8943–8947. CrossRefGoogle Scholar
  28. Grengg C, Mittermayr F, Baldermann A et al (2015) Microbiologically induced concrete corrosion: a case study from a combined sewer network. Cem Concr Res 77:16–25. CrossRefGoogle Scholar
  29. Gutierrez O, Mohanakrishnan J, Sharma KR et al (2008) Evaluation of oxygen injection as a means of controlling sulfide production in a sewer system. Water Res 42:4549–4561. CrossRefGoogle Scholar
  30. Gutierrez O, Park D, Sharma KR, Yuan Z (2009) Effects of long-term pH elevation on the sulfate-reducing and methanogenic activities of anaerobic sewer biofilms. Water Res 43:2549–2557. CrossRefGoogle Scholar
  31. Gutierrez O, Park D, Sharma KR, Yuan Z (2010a) Iron salts dosage for sulfide control in sewers induces chemical phosphorus removal during wastewater treatment. Water Res 44:3467–3475. CrossRefGoogle Scholar
  32. Gutierrez O, Sudarjanto G, Sharma KR et al (2010b) SCORe-CT: a new method for testing effectiveness of sulfide control chemicals used in sewer systems. In: 6th International conference in sewer processes and networks SPN6Google Scholar
  33. Habermann W, Pommer E-H (1991) Biological fuel cells with sulphide storage capacity. Appl Microbiol Biotechnol 35:128–133. CrossRefGoogle Scholar
  34. Harada LK, Silva EC, Campos WF et al (2018) Biotechnological applications of bacteriophages: state of the art. Microbiol Res 212–213:38–58. CrossRefGoogle Scholar
  35. Holmes DE, Bond DR, Lovley DR (2004a) Electron transfer by desulfobulbus propionicus to Fe(III) and Graphite electrodes. Appl Environ Microbiol 70:1234–1237. CrossRefGoogle Scholar
  36. Holmes DE, Bond DR, O’Neil RA et al (2004b) Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microb Ecol 48:178–190. CrossRefGoogle Scholar
  37. Islander RL, Devinny JS, Mansfeld F et al (1991) Microbial ecology of crown corrosion in sewers. J Environ Eng 117:751–770. CrossRefGoogle Scholar
  38. Jassim SAA, Limoges RG, El-Cheikh H (2016) Bacteriophage biocontrol in wastewater treatment. World J Microbiol Biotechnol 32:70. CrossRefGoogle Scholar
  39. Jefferson B, Hurst A, Stuetz R, Parsons SA (2002) A comparison of chemical methods for the control of odours in wastewater. Process Saf Environ Prot 80:93–99. CrossRefGoogle Scholar
  40. Jensen H, Biggs CA, Karunakaran E (2016) The importance of sewer biofilms. WIREs Water 3:487–494. CrossRefGoogle Scholar
  41. Jiang G, Gutierrez O, Sharma KR, Yuan Z (2010) Effects of nitrite concentration and exposure time on sulfide and methane production in sewer systems. Water Res 44:4241–4251. CrossRefGoogle Scholar
  42. Jiang G, Keating A, Corrie S et al (2013) Dosing free nitrous acid for sulfide control in sewers: results of field trials in Australia. Water Res 47:4331–4339. CrossRefGoogle Scholar
  43. Krishnakumar B, Majumdar S, Manilal VB, Haridas A (2005) Treatment of sulphide containing wastewater with sulphur recovery in a novel reverse fluidized loop reactor (RFLR). Water Res 39:639–647. CrossRefGoogle Scholar
  44. Lee DJ, Liu X, Weng HL (2014) Sulfate and organic carbon removal by microbial fuel cell with sulfate-reducing bacteria and sulfide-oxidising bacteria anodic biofilm. Bioresour Technol 156:14–19. CrossRefGoogle Scholar
  45. Lee DJ, Lee C-Y, Chang J-S et al (2015) Treatment of sulfate/sulfide-containing wastewaters using a microbial fuel cell: single and two-anode systems. Int J Green Energy 12:998–1004. CrossRefGoogle Scholar
  46. Liang FY, Deng H, Zhao F (2013) Sulfur pollutants treatment using microbial fuel cells from perspectives of electrochemistry and microbiology. Chin J Anal Chem 41:1133–1139. CrossRefGoogle Scholar
  47. Lin H, Williams N, King A, Hu B (2016) Electrochemical sulfide removal by low-cost electrode materials in anaerobic digestion. Chem Eng J 297:180–192. CrossRefGoogle Scholar
  48. Lin HW, Kustermans C, Vaiopoulou E et al (2017) Electrochemical oxidation of iron and alkalinity generation for efficient sulfide control in sewers. Water Res 118:114–120. CrossRefGoogle Scholar
  49. Liu R, Tursun H, Hou X et al (2017) Microbial community dynamics in a pilot-scale MFC-AA/O system treating domestic sewage. Bioresour Technol 241:439–447. CrossRefGoogle Scholar
  50. Logan B (2008) Introduction. In: Microbial fuel cells. Wiley, Hoboken, NJ, pp 1–12Google Scholar
  51. Lovley DR (2011) Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ Microbiol Rep 3:27–35. CrossRefGoogle Scholar
  52. Lovley DR, Phillips EJP (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480. CrossRefGoogle Scholar
  53. Lovley DR, Giovannoni SJ, White DC et al (1993) Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159:336–344. CrossRefGoogle Scholar
  54. Meaden S, Koskella B (2013) Exploring the risks of phage application in the environment. Front Microbiol 4:1–8. CrossRefGoogle Scholar
  55. Morton RL, Yanko WA, Graham DW, Arnold RG (1991) Relationships between metal concentrations and crown corrosion in Los-Angeles-County sewers. Res J Water Pollut Control Fed 63:789–798Google Scholar
  56. Moskowitz SM, Foster JM, Emerson J et al (2004) Clinically feasible biofilm susceptibility assay for isolates of pseudomonas aeruginosa from patients with cystic fibrosis. J Clin Microbiol 42:1915–1922. CrossRefGoogle Scholar
  57. Muyzer G, Stams AJMM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454. CrossRefGoogle Scholar
  58. Nielsen AH, Lens P, Vollertsen J, Hvitved-Jacobsen T (2005) Sulfide–iron interactions in domestic wastewater from a gravity sewer. Water Res 39:2747–2755. CrossRefGoogle Scholar
  59. Noeiaghaei T, Mukherjee A, Dhami N, Chae S-R (2017) Biogenic deterioration of concrete and its mitigation technologies. Constr Build Mater 149:575–586. CrossRefGoogle Scholar
  60. Okabe S, Ito T, Sugita K, Satoh H (2005) Succession of internal sulfur cycles and sulfur-oxidizing bacterial communities in microaerophilic wastewater biofilms. Appl Environ Microbiol 71:2520–2529. CrossRefGoogle Scholar
  61. Okabe S, Odagiri M, Ito T, Satoh H (2007) Succession of sulfur-oxidizing bacteria in the microbial community on corroding concrete in sewer systems. Appl Environ Microbiol 73:971–980. CrossRefGoogle Scholar
  62. Olmstead WH, Hamlin H (1900) Converting portions of the Los Angeles outfall sewer into a septic tank. Eng News Am Railw J. 44:317–318Google Scholar
  63. Padival NA, Kimbell WA, Redner JA (1995) Use of iron salts to control dissolved sulfide in trunk sewers. J Environ Eng 121:824–829. CrossRefGoogle Scholar
  64. Park K, Lee H, Phelan S et al (2014) Mitigation strategies of hydrogen sulphide emission in sewer networks—a review. Int Biodeterior Biodegrad 95:251–261. CrossRefGoogle Scholar
  65. Petrovski S, Seviour RJ, Tillett D (2011) Prevention of Gordonia and Nocardia stabilized foam formation by using bacteriophage GTE7. Appl Environ Microbiol 77:7864–7867. CrossRefGoogle Scholar
  66. Pikaar I, Rozendal RA, Yuan Z et al (2011) Electrochemical sulfide removal from synthetic and real domestic wastewater at high current densities. Water Res 45:2281–2289. CrossRefGoogle Scholar
  67. Pikaar I, Li E, Rozendal RA et al (2012) Long-term field test of an electrochemical method for sulfide removal from sewage. Water Res 46:3085–3093. CrossRefGoogle Scholar
  68. Pikaar I, Likosova EM, Freguia S et al (2014a) Electrochemical abatement of hydrogen sulfide from waste streams. Crit Rev Environ Sci Technol 45:1555–1578. CrossRefGoogle Scholar
  69. Pikaar I, Sharma KR, Hu S et al (2014b) Reducing sewer corrosion trough integrated urban water management. Science 345:812–814. CrossRefGoogle Scholar
  70. Rabaey K, Clauwaert P, Aelterman P, Verstraete W (2005) Tubular microbial fuel cells for efficient electricity generation. Environ Sci Technol 39:8077–8082. CrossRefGoogle Scholar
  71. Rabaey K, Van de Sompel K, Maignien L et al (2006) Microbial fuel cells for sulfide removal. Environ Sci Technol 40:5218–5224. CrossRefGoogle Scholar
  72. Rauch W, Kleidorfer M (2014) Replace contamination, not the pipes. Science 345:734–735. CrossRefGoogle Scholar
  73. Richter H, McCarthy K, Nevin KP et al (2008) Electricity generation by geobacter sulfurreducens attached to gold electrodes. Langmuir 24:4376–4379CrossRefGoogle Scholar
  74. Rostami A, Akradi J (2010) A highly efficient, green, rapid, and chemoselective oxidation of sulfides using hydrogen peroxide and boric acid as the catalyst under solvent-free conditions. Tetrahedron Lett 51:3501–3503. CrossRefGoogle Scholar
  75. Santo Domingo JW, Revetta RP, Iker B et al (2011) Molecular survey of concrete sewer biofilm microbial communities. Biofouling J Bioadhesion Biofilm Res 27:993–1001. CrossRefGoogle Scholar
  76. Shi X, Xie N, Gong J (2011) Recent progress in the research on microbially influenced corrosion: a Bird’ s eye view through the engineering lens. Recent Patents Corros Sci 1:118–131. CrossRefGoogle Scholar
  77. Shrout JD, Nerenberg R (2012) Monitoring bacterial Twitter: does quorum sensing determine the behavior of water and wastewater treatment biofilms? Environ Sci Technol 46:1995–2005. CrossRefGoogle Scholar
  78. Sudarjanto G, Gutierrez O, Ren G, Yuan Z (2013) Laboratory assessment of bioproducts for sulphide and methane control in sewer systems. Sci Total Environ 443:429–437. CrossRefGoogle Scholar
  79. Summer E, Summer NS (2012) United States Patent No: US 8,241,498 B2—process for remediating biofouling in water systems with virulent bacteriophageGoogle Scholar
  80. Summer EJ, Summer NS, Janes C et al (2011) Phage of sulfate reducing bacteria isolated from high saline environment. In: NACE international corrosion 2011 conference and expo, pp 1–12Google Scholar
  81. Sun M, Mu Z-X, Chen Y-P et al (2009) Microbe-assisted sulfide oxidation in the anode of a microbial fuel cell. Environ Sci Technol 43:3372–3377. CrossRefGoogle Scholar
  82. Talaiekhozani A, Bagheri M, Goli A, Khoozani MRT (2016) An overview of principles of odor production, emission, and control methods in wastewater collection and treatment systems. J Environ Manage 170:186–206. CrossRefGoogle Scholar
  83. ter Heijne A, Hamelers HVM, Saakes M, Buisman CJN (2008) Performance of non-porous graphite and titanium-based anodes in microbial fuel cells. Electrochim Acta 53:5697–5703. CrossRefGoogle Scholar
  84. Tomar M, Abdullah THA (1994) Evaluation of chemicals to control the generation of malodorous hydrogen sulfide in waste water. Water Res 28:2545–2552. CrossRefGoogle Scholar
  85. Vincke E, Boon N, Verstraete W (2001) Analysis of the microbial communities on corroded concrete sewer pipes—a case study. Appl Microbiol Biotechnol 57:776–785. CrossRefGoogle Scholar
  86. Vollertsen J, Nielsen AH, Jensen HS et al (2008) Corrosion of concrete sewers—the kinetics of hydrogen sulfide oxidation. Sci Total Environ 394:162–170. CrossRefGoogle Scholar
  87. Wardman C, Nevin KP, Lovley DR (2014) Real-time monitoring of subsurface microbial metabolism with graphite electrodes. Front Microbiol 5:1–7. CrossRefGoogle Scholar
  88. Wei J, Liang P, Huang X (2011) Recent progress in electrodes for microbial fuel cells. Bioresour Technol 102:9335–9344. CrossRefGoogle Scholar
  89. Wei S, Jiang Z, Liu H et al (2013) Microbiologically induced deterioration of concrete—a review. Braz J Microbiol 44:1001–1007. CrossRefGoogle Scholar
  90. Wells T, Melchers RE (2014) An observation-based model for corrosion of concrete sewers under aggressive conditions. Cem Concr Res 61–62:1–10. CrossRefGoogle Scholar
  91. Wells T, Melchers RE (2015) Modelling concrete deterioration in sewers using theory and field observations. Cem Concr Res 77:82–96. CrossRefGoogle Scholar
  92. Wells T, Melchers RE, Bond P (2009) Factors involved in the long term corrosion of concrete sewers. In: 49th Annual conference of the Australasian corrosion association 2009: corrosion and prevention 2009, pp 345–356Google Scholar
  93. Wells T, Melchers R, Joseph A et al (2012) A collaborative investigation of microbial corrosion of concrete sewer pipe in Australia. In: Proceedings of OzWater-12 Australia's National Water Conference and Exhibition, Sydney, NSW, pp 8–10Google Scholar
  94. Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5:226–235. CrossRefGoogle Scholar
  95. Wu H, Moser C, Wang H-Z et al (2015) Strategies for combating bacterial biofilm infections. Int J Oral Sci 7:1–7. CrossRefGoogle Scholar
  96. Wu B, Wang R, Fane AG (2017) The roles of bacteriophages in membrane-based water and wastewater treatment processes: a review. Water Res 110:120–132. CrossRefGoogle Scholar
  97. Yongsiri C, Vollertsen J, Hvitved-Jacobsen T (2004) Hydrogen sulfide emission in sewer networks: a two phase modelling approach to the sulfur cycle. Water Sci Technol 50:161–168. CrossRefGoogle Scholar
  98. Zarasvand KA, Rai VR (2014) Microorganisms: induction and inhibition of corrosion in metals. Int Biodeterior Biodegrad 87:66–74. CrossRefGoogle Scholar
  99. Zhang L, De Schryver P, De Gusseme B et al (2008) Chemical and biological technologies for hydrogen sulfide emission control in sewer systems: a review. Water Res 42:1–12. CrossRefGoogle Scholar
  100. Zhou M, Chi M, Luo J et al (2011) An overview of electrode materials in microbial fuel cells. J Power Sources 196:4427–4435. CrossRefGoogle Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Physiology, Anatomy and MicrobiologyLa Trobe UniversityMelbourneAustralia
  2. 2.Western WaterSunburyAustralia
  3. 3.Centre for Future LandscapesLa Trobe UniversityMelbourneAustralia
  4. 4.Securing Food, Water and Environment Research Focus AreaLa Trobe UniversityMelbourneAustralia

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