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

Aminov RI (2010) A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 1:1–7. https://doi.org/10.3389/fmicb.2010.00134 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. https://doi.org/10.1128/AEM.69.10.5884 Bergel A, Féron D, Mollica A (2005) Catalysis of oxygen reduction in PEM fuel cell by seawater biofilm. Electrochem Commun 7:900–904. https://doi.org/10.1016/j.elecom.2005.06.006 Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485. https://doi.org/10.1126/science.1066771 Bradley AS, Leavitt WD, Johnston DT (2011) Revisiting the dissimilatory sulfate reduction pathway. Geobiology 9:446–457. https://doi.org/10.1111/j.1472-4669.2011.00292.x 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. https://doi.org/10.1016/j.rser.2015.08.058 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. https://doi.org/10.1016/j.seppur.2014.07.024 Candena F, Peters RW (1988) Evaluation of chemical oxidizers for hydrogen sulfide control. J Water Pollut Control Fed 60:1259–1263 Chambers LA, Trudinger PA (1975) Are thiosulfate and trithionate intermediates in dissimilatory sulfate reduction? J Bacteriol 123:36–40 Cheng S, Logan BE (2007) Ammonia treatment of carbon cloth anodes to enhance power generation of microbial fuel cells. Electrochem Commun 9:492–496. https://doi.org/10.1016/j.elecom.2006.10.023 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. https://doi.org/10.1016/j.ijhydene.2013.04.074 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. https://doi.org/10.1016/j.ijhydene.2014.03.236 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. https://doi.org/10.1016/j.ces.2006.07.030 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. https://doi.org/10.1016/j.electacta.2007.06.069 Dutta PK, Rozendal RA, Yuan Z et al (2009) Electrochemical regeneration of sulfur loaded electrodes. Electrochem Commun 11:1437–1440. https://doi.org/10.1016/j.elecom.2009.05.024 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. https://doi.org/10.1007/s00449-012-0881-3 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. https://doi.org/10.1016/j.bios.2010.05.006 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. https://doi.org/10.1016/j.scitotenv.2007.11.008 Frechen F-B, Romaker J, Giebel SM (2014) Controlling chemical dosing into sewers for odour and corrosion abatement. Chem Eng Trans 40:217–222. https://doi.org/10.3303/CET1440037 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. https://doi.org/10.1061/(asce)ee.1943-7870.0001151 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. https://doi.org/10.1061/(ASCE)EE.1943-7870.0000650 Goldnik E, Turek T (2016) Removal of hydrogen sulfide by permanganate based sorbents: experimental investigation and reactor modeling. Chem Eng Sci 151:51–63. https://doi.org/10.1016/j.ces.2016.04.059 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. https://doi.org/10.1186/1471-2180-12-122 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. https://doi.org/10.1139/cjm-2015-0142 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. https://doi.org/10.1139/cjm-2012-0245 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. https://doi.org/10.3382/ps.2013-03520 Gregory KB, Lovley DR (2005) Remediation and recovery of uranium from contaminated subsurface environments with electrodes. Environ Sci Technol 39:8943–8947. https://doi.org/10.1021/es050457e 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. https://doi.org/10.1016/j.cemconres.2015.06.011 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. https://doi.org/10.1016/j.watres.2008.07.042 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. https://doi.org/10.1016/j.watres.2009.03.008 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. https://doi.org/10.1016/j.watres.2010.03.023 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 SPN6 Habermann W, Pommer E-H (1991) Biological fuel cells with sulphide storage capacity. Appl Microbiol Biotechnol 35:128–133. https://doi.org/10.1007/BF00180650 Harada LK, Silva EC, Campos WF et al (2018) Biotechnological applications of bacteriophages: state of the art. Microbiol Res 212–213:38–58. https://doi.org/10.1016/j.micres.2018.04.007 Holmes DE, Bond DR, Lovley DR (2004a) Electron transfer by desulfobulbus propionicus to Fe(III) and Graphite electrodes. Appl Environ Microbiol 70:1234–1237. https://doi.org/10.1128/AEM.70.2.1234-1237.2004 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. https://doi.org/10.1007/s00248-003-0004-4 Islander RL, Devinny JS, Mansfeld F et al (1991) Microbial ecology of crown corrosion in sewers. J Environ Eng 117:751–770. https://doi.org/10.1061/(ASCE)0733-9372(1991)117:6(751) Jassim SAA, Limoges RG, El-Cheikh H (2016) Bacteriophage biocontrol in wastewater treatment. World J Microbiol Biotechnol 32:70. https://doi.org/10.1007/s11274-016-2028-1 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. https://doi.org/10.1205/095758202753553211 Jensen H, Biggs CA, Karunakaran E (2016) The importance of sewer biofilms. WIREs Water 3:487–494. https://doi.org/10.1002/wat2.1144 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. https://doi.org/10.1016/j.watres.2010.05.030 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. https://doi.org/10.1016/j.watres.2013.05.024 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. https://doi.org/10.1016/j.watres.2004.11.015 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. https://doi.org/10.1016/j.biortech.2013.12.129 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. https://doi.org/10.1080/15435075.2014.910780 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. https://doi.org/10.1016/S1872-2040(13)60669-6 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. https://doi.org/10.1016/j.cej.2016.03.086 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. https://doi.org/10.1016/j.watres.2017.02.069 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. https://doi.org/10.1016/j.biortech.2017.05.122 Logan B (2008) Introduction. In: Microbial fuel cells. Wiley, Hoboken, NJ, pp 1–12 Lovley DR (2011) Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ Microbiol Rep 3:27–35. https://doi.org/10.1111/j.1758-2229.2010.00211.x 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. https://doi.org/10.1103/PhysRevLett.50.1998 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. https://doi.org/10.1007/BF00290916 Meaden S, Koskella B (2013) Exploring the risks of phage application in the environment. Front Microbiol 4:1–8. https://doi.org/10.3389/fmicb.2013.00358 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 63:789–798 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. https://doi.org/10.1128/JCM.42.5.1915 Muyzer G, Stams AJMM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454. https://doi.org/10.1038/nrmicro1892 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. https://doi.org/10.1016/j.watres.2005.04.048 Noeiaghaei T, Mukherjee A, Dhami N, Chae S-R (2017) Biogenic deterioration of concrete and its mitigation technologies. Constr Build Mater 149:575–586. https://doi.org/10.1016/j.conbuildmat.2017.05.144 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. https://doi.org/10.1128/AEM.71.5.2520-2529.2005 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. https://doi.org/10.1128/AEM.02054-06 Olmstead WH, Hamlin H (1900) Converting portions of the Los Angeles outfall sewer into a septic tank. Eng News Am Railw J. 44:317–318 Padival NA, Kimbell WA, Redner JA (1995) Use of iron salts to control dissolved sulfide in trunk sewers. J Environ Eng 121:824–829. https://doi.org/10.1061/(ASCE)0733-9372(1995)121:11(824) 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. https://doi.org/10.1016/j.ibiod.2014.02.013 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. https://doi.org/10.1128/AEM.05692-11 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. https://doi.org/10.1016/j.watres.2010.12.025 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. https://doi.org/10.1016/j.watres.2012.03.013 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. https://doi.org/10.1080/10643389.2014.966419 Pikaar I, Sharma KR, Hu S et al (2014b) Reducing sewer corrosion trough integrated urban water management. Science 345:812–814. https://doi.org/10.1126/science.1251418 Rabaey K, Clauwaert P, Aelterman P, Verstraete W (2005) Tubular microbial fuel cells for efficient electricity generation. Environ Sci Technol 39:8077–8082. https://doi.org/10.1021/es050986i Rabaey K, Van de Sompel K, Maignien L et al (2006) Microbial fuel cells for sulfide removal. Environ Sci Technol 40:5218–5224. https://doi.org/10.1021/es060382u Rauch W, Kleidorfer M (2014) Replace contamination, not the pipes. Science 345:734–735. https://doi.org/10.1126/science.1258654 Richter H, McCarthy K, Nevin KP et al (2008) Electricity generation by geobacter sulfurreducens attached to gold electrodes. Langmuir 24:4376–4379 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. https://doi.org/10.1016/j.tetlet.2010.04.103 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. https://doi.org/10.1080/08927014.2011.618637 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. https://doi.org/10.2174/1877610811101020118 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. https://doi.org/10.1021/es203933h 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. https://doi.org/10.1016/j.scitotenv.2012.10.083 Summer E, Summer NS (2012) United States Patent No: US 8,241,498 B2—process for remediating biofouling in water systems with virulent bacteriophage 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 1–12 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. https://doi.org/10.1021/es802809m 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. https://doi.org/10.1016/j.jenvman.2016.01.021 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. https://doi.org/10.1016/j.electacta.2008.03.032 Tomar M, Abdullah THA (1994) Evaluation of chemicals to control the generation of malodorous hydrogen sulfide in waste water. Water Res 28:2545–2552. https://doi.org/10.1016/0043-1354(94)90072-8 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. https://doi.org/10.1007/s002530100826 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. https://doi.org/10.1016/j.scitotenv.2008.01.028 Wardman C, Nevin KP, Lovley DR (2014) Real-time monitoring of subsurface microbial metabolism with graphite electrodes. Front Microbiol 5:1–7. https://doi.org/10.3389/fmicb.2014.00621 Wei J, Liang P, Huang X (2011) Recent progress in electrodes for microbial fuel cells. Bioresour Technol 102:9335–9344. https://doi.org/10.1016/j.biortech.2011.07.019 Wei S, Jiang Z, Liu H et al (2013) Microbiologically induced deterioration of concrete—a review. Braz J Microbiol 44:1001–1007. https://doi.org/10.1590/S1517-83822014005000006 Wells T, Melchers RE (2014) An observation-based model for corrosion of concrete sewers under aggressive conditions. Cem Concr Res 61–62:1–10. https://doi.org/10.1016/j.cemconres.2014.03.013 Wells T, Melchers RE (2015) Modelling concrete deterioration in sewers using theory and field observations. Cem Concr Res 77:82–96. https://doi.org/10.1016/j.cemconres.2015.07.003 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 345–356 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 8–10 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. https://doi.org/10.4161/viru.25991 Wu H, Moser C, Wang H-Z et al (2015) Strategies for combating bacterial biofilm infections. Int J Oral Sci 7:1–7. https://doi.org/10.1038/ijos.2014.65 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. https://doi.org/10.1016/j.watres.2016.12.004 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. https://doi.org/10.2166/wst.2004.0251 Zarasvand KA, Rai VR (2014) Microorganisms: induction and inhibition of corrosion in metals. Int Biodeterior Biodegrad 87:66–74. https://doi.org/10.1016/j.ibiod.2013.10.023 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. https://doi.org/10.1016/j.watres.2007.07.013 Zhou M, Chi M, Luo J et al (2011) An overview of electrode materials in microbial fuel cells. J Power Sources 196:4427–4435. https://doi.org/10.1016/j.jpowsour.2011.01.012