Abstract
Industrial by-products and wastes from Portugal and Spain were tested for the first time as carbon sources/electron donors for sulphate-reducing bacteria. Cultures in mineral medium supplemented with the tested substrates were monitored, and sulphate reduction efficiency is discussed in light of substrates compositions, dosages and corresponding chemical oxygen demand/[SO42−] ratios. The results reveal the ability of those substrates to feed SRB and confirm that testing doses targeting ratios of 1.5 and values close to this was a good strategy to optimize sulphate reduction activity. As expected, this activity was faster for substrates that have in their composition simple compounds (such as low-chain alcohols and organic acids) and/or compounds that can be rapidly degraded (such as sugars), though it also occurred in a longer-term perspective with substrates composed mainly of slowly degradable compounds (such as cellulose and lignin). Thus, this work demonstrates the potential of new substrates and respective required doses to feed SRB bioreactors in long-term passive bioremediation processes or faster more active processes. That is, it opens the way for the use of such substrates in the treatment of sulphate-rich waters, as the acid mine drainage generated in some mines on the Iberian Pyrite Belt region, and it encourages further experiments to evaluate the use of SRB-based processes to treat the industrial wastewaters successfully tested in this work themselves, specially the olive mill wastewater which is still a problem for many small olive oil producers.
Similar content being viewed by others
References
Almendros AI, Martín-Lara MA, Ronda A, Pérez A, Blázquez G, Calero M (2015) Physico-chemical characterization of pine cone shell and its use as biosorbent and fuel. Bioresour Technol 196:406–412. https://doi.org/10.1016/j.biortech.2015.07.109
Amaral C, Lucas MS, Coutinho J, Crespí AL, do Rosário Anjos M, Pais C (2008) Microbiological and physicochemical characterization of olive mil wastewaters from a continuous olive mill in Northeastern Portugal. Bioresour Technol 99:7215–7223. https://doi.org/10.1016/j.biortech.2007.12.058
Annachhatre AP, Suktrakoolvait S (2001) Biological sulphate reducing using molasses as a carbon source. Water Environ Res 73:118–126. https://doi.org/10.2175/106143001X138778
Azbar N, Bayram A, Filibeli A, Muezzinoglu A, Sengul F, Ozer A (2004) A review of wastes management options in olive oil production. Crit Rev Environ Sci Technol 34:209–247. https://doi.org/10.1080/10643380490279932
Baena S, Fardeau ML, Labat M, Ollivier B, Garcia JL, Patel BKC (1998) Desulfovibrio aminophilus sp. nov., a novel amino acid degrading and sulfate reducing bacterium from an anaerobic dairy wastewater lagoon. Syst Appl Microbiol 21(4):498–504. https://doi.org/10.1016/S0723-2020(98)80061-1
Bechard G, Yamazaki H, Gould WD, Bedard P (1994) Use of cellulosic substrates for the microbial treatment of acid mine drainage. J Environ Qual 23:111–116. https://doi.org/10.2134/jeq1994.00472425002300010017x
Buzzini AP, Pires EC (2007) Evaluation of a upflow anaerobic sludge blanket reactor with partial recirculation of effluent used to treat wastewaters from pulp and paper plants. Bioresour Technol 98:1838–1848. https://doi.org/10.1016/j.biortech.2006.06.030
Cao J, Zhang G, Mao Z, Li Y, Fang F, Chao Y (2012) Influence of electron donors on the growth and activity of sulphate-reducing bacteria. Int J Miner Process 106–109:58–64. https://doi.org/10.1016/j.minpro.2012.02.005
Castro JM, Moore JN (2000) Pit lakes: their characteristics and the potential for their remediation. Environ Geol 39:1254–1260. https://doi.org/10.1007/s002549900100
Chamkh F, Spröer C, Lemos PC, Besson S, El Asli AG, Bennisse R, Labat M, Reis M, Qatibi AI (2009) Desulfovibrio marrakechensis sp. nov., a 1,4-tyrosol-oxidizing, sulphate-reducing bacterium isolated from olive mill wastewater. Int J Syst Evol Microbiol 59:936–942. https://doi.org/10.1099/ijs.0.003822-0
Chen W, Horan NJ (1998) The treatment of a high strength pulp and paper mill effluent for wastewater re-use. Environ Technol 19:163–171. https://doi.org/10.1080/09593330.1998.9618627
Choudhary RP, Sheoran AS (2011) Comparative study of cellulose waste versus organic waste as substrate in a sulphate reducing bioreactor. Bioresour Technol 102:4319–4324. https://doi.org/10.1016/j.biortech.2010.08.126
Clements RL (1964) Organic acids in citrus fruits. I. Varietal differences. J Food Sci 29:276–280. https://doi.org/10.1111/j.1365-2621.1964.tb01731.x
Costa MC, Duarte JC (2005) Bioremediation of acid mine drainage using acidic soil and organic wastes for promoting sulphate-reducing bacteria activity on a column reactor. Water Air Soil Pollut 165:325–345. https://doi.org/10.1007/s11270-005-6914-7
Costa JM, Rodriguez RP, Sancinetti GP (2017) Removal sulfate and metals Fe+2, Cu+2, and Zn+2 from acid mine drainage in an anaerobic sequential batch reactor. J Environ Chem Eng 5(2):1985–1989. https://doi.org/10.1016/j.jece.2017.04.011
Das BK, Gauri SS, Bhattacharya J (2013) Sweetmeat waste fractions as suitable organic carbon source for biological sulfate reduction. Int Biodeterior Biodegrad 82:215–223. https://doi.org/10.1016/j.ibiod.2013.03.027
Dev S, Roy S, Bhattacharya J (2017) Optimization of the operation of packed bed bioreactor to improve the sulfate and metal removal from acid mine drainage. J Environ Manag 200:135–144. https://doi.org/10.1016/j.jenvman.2017.04.102
Elliott P, Ragusa S, Catcheside D (1998) Growth of sulphate-reducing bacteria under acidic conditions in an upflow anaerobic bioreactor as a treatment system for acid mine drainage. Water Res 32:3724–3730. https://doi.org/10.1016/S0043-1354(98)00144-4
Hao T, Xiang P, Mackey HR, Chi K, Lu H, Chui H, van Loosdrecht MCM, Chen GH (2014) A review of biological sulphate conversions in wastewater treatment. Water Res 65:1–21. https://doi.org/10.1016/j.mineng.2016.02.008
Hokkanen S, Bhatnagar A, Sillanpää M (2016) A review on modification methods to cellulose-based adsorbents to improve adsorption capacity. Water Res 91:156–173. https://doi.org/10.1016/j.watres.2016.01.008
Hussain A, Qazi JI (2012) Biological sulphate reduction using watermelon rind as a carbon source. Biologia (Pakistan) 58:85–92
Hussain A, Qazi J (2016) Application of sugarcane bagasse for passive anaerobic biotreatment of sulphate rich wastewaters. Appl Water Sci 6(2):205–211. https://doi.org/10.1007/s13201-014-0226-2
Jiang Y, Qin Y, Yu F, Li H, Liu K (2018) Is COD/SO4 2− ratio responsible for metabolic phase-separation shift in anaerobic baffled reactor treating sulfate-laden wastewater? Int Biodeterior Biodegrad 126:37–44. https://doi.org/10.1016/j.ibiod.2017.08.013
Kim YM, Kim S, Han TU, Park YK, Watanabe C (2014) Pyrolysis reaction characteristics of Korean pine (Pinus Koraiensis) nut shell. J Anal Appl Pyrol 110:435–441. https://doi.org/10.1016/j.jaap.2014.10.013
Kiran MG, Pakshirajan K, Das G (2017) An overview of sulfidogenic biological reactors for the simultaneous treatment of sulfate and heavy metal rich wastewater. Chem Eng Sci 158:606–620. https://doi.org/10.1016/j.ces.2016.11.002
Kiyuna LS, Fuess LT, Zaiat M (2017) Unraveling the influence of the COD/sulfate ratio on organic matter removal and methane production from the biodigestion of sugarcane vinasse. Bioresour Technol 232:103–112. https://doi.org/10.1016/j.biortech.2017.02.028
Koschorreck M, Wendt-Potthoff K, Bozau E, Herzsprung P, Geller W, Schultze M (2007) In: Cidu R, Frau F (eds) IMWA symposium 2007: Water in mining environments. OAI, Cagliari, Italy, 27–31st May 2007
Kumar RN, McCullough CD, Lund MA (2011) How does storage affect the quality and quantity of organic carbon in sewage for use in the bioremediation of acidic mine waters? Ecol Eng 37:1205–1213. https://doi.org/10.1016/j.ecoleng.2011.02.021
Lefticariu L, Walters ER, Pugh CW, Bender KS (2015) Sulfate reducing bioreactor dependence on organic substrates for remediation of coal-generated acid mine drainage: field experiments. Appl Geochem 63:70–82. https://doi.org/10.1016/j.apgeochem.2015.08.002
Li YL, Wang J, Yue ZB, Tao W, Yang HB, Zhou YF, Chen TH (2017) Simultaneous chemical oxygen demand removal, methane production and heavy metal precipitation in the biological treatment of landfill leachate using acid mine drainage as sulfate resource. J Biosci Bioeng 124(1):71–75. https://doi.org/10.1016/j.jbiosc.2017.02.009
Liamleam W, Annachatre AP (2007) Electron donors for biological sulfate reduction. Biotechnol Adv 25:452–463. https://doi.org/10.1016/j.biotechadv.2007.05.002
Logan MV, Reardon KF, Figueroa LA, McLain JET, Ahmann DM (2005) Microbial community activities during establishment, performance, and decline of bench-scale passive treatment systems for mine drainage. Water Res 39:4537–4551. https://doi.org/10.1016/j.watres.2005.08.013
Lowson RT (1982) Aqueous oxidation of pyrite by molecular oxygen. Chem Rev 82:461–497. https://doi.org/10.1021/cr00051a001
Lu X, Zhen G, Ni J, Kubota K, Li YY (2017) Sulfidogenesis process to strengthen re-granulation for biodegradation of methanolic wastewater and microorganisms evolution in an UASB reactor. Water Res 108:137–150. https://doi.org/10.1016/j.watres.2016.10.073
MacPherson R, Miller JDA (1963) Nutritional studies on Desulfovibrio desulfuricuns using chemically defined media. Microbiology 31:365–373. https://doi.org/10.1099/00221287-31-3-365
Maree JP, Gerber A, Hill E (1987) An integrated process for biological treatment of sulphate-containing industrial effluents. J Water Pollut Control Fed 59:1069–1074
Martins M, Faleiro ML, Barros RJ, Veríssimo AR, Costa MC (2009) Biological sulphate reduction using food industry wastes as carbon sources. Biodegradation 20:559–567. https://doi.org/10.1007/s10532-008-9245-8
Michailides MK, Tekerlekopoulou AG, Akratos CS, Coles S, Pavlou S, Vayenas DV (2015) Molasses as an efficient low-cost carbon source for biological Cr(VI) removal. J Hazard Mater 8:95–105. https://doi.org/10.1016/j.jhazmat.2014.08.004
Miran W, Jang J, Nawaz M, Shahzad A, Jeong SE, Jeon CO, Lee DS (2017) Mixed sulfate-reducing bacteria-enriched microbial fuel cells for the treatment of wastewater containing copper. Chemosphere 189:134–142. https://doi.org/10.1016/j.chemosphere.2017.09.048
Muhammad SN, Kusin FM, Madzin Z (2017) Coupled physicochemical and bacterial reduction mechanisms for passive remediation of sulfate- and metal-rich acid mine drainage. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-017-1594-6
Mulopo J (2016) Pilot scale assessment of the continuous biological sulphate removal from coal acid mine effluent using grass cutting as carbon and energy sources. J Water Process Eng 11:104–109. https://doi.org/10.1016/j.jwpe.2016.04.001
Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6(6):441–454. https://doi.org/10.1038/nrmicro1892
Neculita CM, Zagury GJ (2008) Biological treatment of highly contaminated acid mine drainage in batch reators: long-term treatment and reactive mixture characterization. J Hazard Mater 157:359–366. https://doi.org/10.1016/j.jhazmat.2008.01.002
Neculita CM, Zagury GJ, Bussiere B (2007) Passive treatment of acid mine drainage in bioreactors using sulphate-reducing bacteria: critical review and research needs. J Environ Qual 36:1–16. https://doi.org/10.2134/jeq2006.0066
O’Flaherty V, Mahony T, O’Kennedy R, Colleran E (1998) Effect of pH on growth kinetics and sulphide toxicity thresholds of a range of methanogenic, syntrophic and sulphate-reducing bacteria. Process Biochem 33(5):555–569. https://doi.org/10.1016/S0032-9592(98)00018-1
Ollivier B, Cord-Ruwisch R, Hatchikian EC, Garcia JL (1988) Characterization of Desulfovibrio fructosovorans sp. nov. Arch Microbiol 149:447–450. https://doi.org/10.1007/BF00425586
Parshina SN, Sipma J, Henstra AM, Stams AJ (2010) Carbon monoxide as an electron donor for the biological reduction of sulphate. Int J Microbiol 2010:319527. https://doi.org/10.1155/2010/319527
Pereira R, Ribeiro R, Gonçalves F (2004) Plan for an integrated human and environmental risk assessment in the S. Domingos mine area (Portugal). Hum Ecol Risk Assess 10:543–578. https://doi.org/10.1080/10807030490452197
Postgate JR (1984) The sulphate-reducing bacteria, 2nd edn. Cambridge University Press, Cambridge
Prasad D, Wai M, Bérubé P, Henry JG (1999) Evaluating substrates in the biological treatment of acid mine drainage. Environ Technol 20:449–458. https://doi.org/10.1080/09593332008616840
Prasetyo EN, Rodríguez RD, Lukesch B, Weiss S, Murkovic M, Katsoyannos E, Sygmund C, Ludwig R, Nyanhongo GS, Guebitz GM (2015) Laccase–cellobiose dehydrogenase-catalyzed detoxification of phenolic-rich olive processing residues. Int J Environ Sci Technol 12:1343–1352. https://doi.org/10.1007/s13762-014-0526-y
Rambabu N, Panthapulakkal S, Sain M, Dalai AK (2016) Production of nanocellulose fibers from pinecone biomass: evaluation and optimization of chemical and mechanical treatment conditions on mechanical properties of nanocellulose films. Ind Crop Prod 83:746–754. https://doi.org/10.1016/j.indcrop.2015.11.083
Raunkjaer K, Jacobsen TH, Nielsen PH (1994) Measurement of pools of protein, carbohydrate and lipid in domestic wastewater. Water Res 28:251–262. https://doi.org/10.1016/0043-1354(94)90261-5
Relvas JMRS, Barriga FJAS, Longstaffe FJ (2006) Hydrothermal alteration and mineralization in the Neves-Corvo volcanic-hosted massive sulfide deposit, Portugal. II. Oxygen, hydrogen, and carbon isotopes. Econ Geol 101(4):791–804. https://doi.org/10.2113/gsecongeo.101.4.791
Rivas B, Torrado A, Torre P, Converti A, Dominguez JM (2008) Submerged citric acid fermentation on orange peel autohydrolysate. J Agric Food Chem 56:2380–2387. https://doi.org/10.1021/jf073388r
Shofinita D, Feng S, Langrish TAG (2015) Comparing yields from the extraction of different citrus peels and spray drying of the extracts. Adv Powder Technol 26:1633–1638. https://doi.org/10.1016/j.apt.2015.09.007
van Haandel AC, van der Lubbe JGM (2007) Handbook biological waste water treatment—design and optimization of activated sludge systems. Quist Publishing, Leidschendam
Vasquez Y, Escobar MC, Neculita CM, Arbeli Z, Roldan F (2016) Selection of reactive mixture for biochemical passive treatment of acid mine drainage. Environ Earth Sci 75:576. https://doi.org/10.1007/s12665-016-5374-2
Vela FJ, Zaiat M, Foresti E (2002) Influence of the COD to sulphate ratio on the anaerobic organic matter degradation kinetics. Water SA 28:213–216. https://doi.org/10.4314/wsa.v28i2.4887
Wang A, Ren N, Wang X, Lee D (2008) Enhanced sulphate reduction with acidogenic sulphate-reducing bacteria. J Hazard Mater 154:1060–1065. https://doi.org/10.1016/j.jhazmat.2007.11.022
Willow MA, Cohen RRH (2003) pH, dissolved oxygen, and adsorption effects on metal removal in anaerobic bioreactors. J Environ Qual 32:1212–1221. https://doi.org/10.2134/jeq2003.1212
Wolicka D, Borkowski A (2009) Phosphogypsum biotransformation in cultures of sulphate reducing bacteria in whey. Int Biodeterior Biodegrad 63:322–327. https://doi.org/10.1016/j.ibiod.2008.09.011
Zerrouki S, Rihani R, Bentahar F, Belkacemi K (2015) Anaerobic digestion of wastewater from the fruit juice industry: experiments and modeling. Water Sci Technol 72:123–134. https://doi.org/10.2166/wst.2015.193
Zhang M, Wang H (2014) Organic wastes as carbon sources to promote sulphate reducing bacterial activity for biological remediation of acid mine drainage. Miner Eng 69:81–90. https://doi.org/10.1016/j.mineng.2014.07.010
Zhang QH, Jin PK, Ngo HH, Shi X, Guo WS, Yang SJ, Wang XC, Wang X, Dzakpasu M, Yang WN, Yang L (2016) Transformation and utilization of slowly biodegradable organic matters in biological sewage treatment of anaerobic anoxic oxic systems. Bioresour Technol 218:53–61. https://doi.org/10.1016/j.biortech.2016.06.068
Acknowledgements
The authors also wish to acknowledge the company Águas do Algarve, namely Eng. Joaquim Freire and Eng. Patrício Fontinha, for supplying the WWTP sludge used to enrich cultures with SRB and companies that supplied the substrates tested as sources of carbon sources/electron donors (and the persons involved in this supply): Orange juice plant LARA—Laranja do Algarve S.A. (Eng. Pedro Pacheco), Factory of candies Dulciora (anonymous collaboration), Sugar processing plant Azucarera (Eng. Maria Hernandez Garcia), Olive mill Lagar Santa Catarina (Eng. Renato Rocha), Águas Públicas do Alentejo, WWTP Mina de São Domingos (Eng. Olga Martins), Paper and paper pulp factories Navigator Company (Eng. Luis Medeiros Machado and Eng. Patrícia Castellano Rodrigues).
Funding
The research leading to these results has received funding from the European Union’s Seventh Framework Programme (FP7/2007-2013) managed by REA-Research Executive Agency (http://ec.europa.eu/research/rea) under Grant Agreement No. 619101; and the Portuguese Foundation for Science and Technology (FCT) through the Project UID/Multi/04326/2019.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Editorial responsibility: M. Abbaspour.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Carlier, J.D., Alexandre, L.M., Luís, A.T. et al. Potential of industrial by-products and wastes from the Iberian Peninsula as carbon sources for sulphate-reducing bacteria. Int. J. Environ. Sci. Technol. 16, 4719–4738 (2019). https://doi.org/10.1007/s13762-018-02197-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13762-018-02197-z




