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Microrespirometric characterization of activated sludge inhibition by copper and zinc

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Abstract

We have developed a novel microrespirometric method to characterize the inhibitory effects due to heavy metals on activated sludge treatment. This method was based on pulse dynamic respirometry and involved the injection of several pulses of substrate and inhibitors, of increasing concentration. Furthermore, we evaluated the inhibitory effects of heavy metals (copper and zinc), substrate and biomass concentrations, and pH on activated sludge activity. While higher biomass concentrations counteracted the inhibitory effects of both copper and zinc, higher substrate concentrations predominantly augmented the inhibitory effect of copper but no significant change in inhibition by zinc was observed. pH had a clear but relatively small effect on inhibition, partially explained by thermodynamic speciation. We determined the key kinetic parameters; namely, the half saturation constant (K S ) and the maximum oxygen uptake rate (OUR max ). The results showed that higher heavy metal concentrations substantially decreased K S and OUR max suggesting that the inhibition was uncompetitive.

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References

  • AdS Oliveira, Bocio A, Trevilato TMB, Takayanagui AMM, Doming JL, Segura-Munoz SI (2007) Heavy metals in untreated/treated urban effluent and sludge from a biological wastewater treatment plant. Environ Sci Pollut Res 14(7):483–489. doi:10.1065/espr2006.10.355

    Article  Google Scholar 

  • Ahluwalia SS, Goyal D (2007) Microbial and plant derived biomass for removal of heavy metals from wastewater. Bioresour Technol 98(12):2243–2257. doi:10.1016/j.biortech.2005.12.006

    Article  PubMed  CAS  Google Scholar 

  • Algarra M, Jimenez MV, Rodriguez-Castellon E, Jimenez-Lopez A, Jimenez-Jimenez J (2005) Heavy metals removal from electroplating wastewater by aminopropyl-Si MCM-41. Chemosphere 59(6):779–786. doi:10.1016/j.chemosphere.2004.11.023

    Article  PubMed  CAS  Google Scholar 

  • Alkan U, Eleren SC, Nalbur BE, Odabas E (2008) Influence of the activated sludge system configuration on heavy metal toxicity reduction. World J Microbiol Biotechnol 24(8):1435–1443. doi:10.1007/s11274-007-9629-7

    Article  CAS  Google Scholar 

  • Alonso E, Santos A, Callejon M, Jimenez JC (2004) Speciation as a screening tool for the determination of heavy metal surface water pollution in the Guadiamar river basin. Chemosphere 56(6):561–570. doi:10.1016/j.chemosphere.2004.04.031

    Article  PubMed  CAS  Google Scholar 

  • APHA (1999) Standard methods for the examination of water and wastewater, 20th edn. American Publishers Health Association, Washington DC

    Google Scholar 

  • Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45(3):198–207. doi:10.1006/eesa.1999.1860

    Article  PubMed  CAS  Google Scholar 

  • Carvallo L, Carrera J, Chamy R (2002) Nitrifying activity monitoring and kinetic parameters determination in a biofilm airlift reactor by respirometry. Biotechnol Lett 24(24):2063–2066. doi:10.1023/a:1021375523879

    Article  CAS  Google Scholar 

  • Cecen F, Semerci N, Geyik AG (2010) Inhibitory effects of Cu, Zn, Ni and Co on nitrification and relevance of speciation. J Chem Technol Biotechnol 85(4):520–528. doi:10.1002/jctb.2321

    CAS  Google Scholar 

  • Cokgor EU, Wdemir S, Karahan O, Insel G, Orhon D (2007) Critical appraisal of respirometric methods for metal inhibition on activated sludge. J Hazard Mater 139(2):332–339. doi:10.1016/j.jhazmat.2006.06.038

    Article  PubMed  Google Scholar 

  • Development Core Team R (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • El Bestawy E, Helmy S, Hussein H, Fahmy M (2013) Optimization and/or acclimatization of activated sludge process under heavy metals stress. World J Microbiol Biotechnol 29(4):693–705. doi:10.1007/s11274-012-1225-9

    Article  PubMed  Google Scholar 

  • Esquivel-Rios I, Ramirez-Vargas R, Hernandez-Martinez GR, Vital-Jacome M, Ordaz A, Thalasso F (2014) A microrespirometric method for the determination of stoichiometric and kinetic parameters of heterotrophic and autotrophic cultures. Biochem Eng J 83:70–78

    Article  CAS  Google Scholar 

  • Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manage 92(3):407–418. doi:10.1016/j.jenvman.2010.11.011

    Article  PubMed  CAS  Google Scholar 

  • Gernaey AK, Petersen B, Ottoy JP, Vanrolleghem P (2001) Activated sludge monitoring with combined respirometric-titrimetric measurements. Water Res 35(5):1280–1294. doi:10.1016/s0043-1354(00)00366-3

    Article  CAS  Google Scholar 

  • Gikas P (2007) Kinetic responses of activated sludge to individual and joint nickel (Ni(II)) and cobalt (Co(II)): an isobolographic approach. J Hazard Mater 143(1–2):246–256. doi:10.1016/j.jhazmat.2006.09.019

    Article  PubMed  CAS  Google Scholar 

  • Gikas P (2008) Single and combined effects of nickel (Ni(II)) and cobalt (Co(II)) ions on activated sludge and on other aerobic microorganisms: a review. J Hazard Mater 159(2–3):187–203. doi:10.1016/j.jhazmat.2008.02.048

    Article  PubMed  CAS  Google Scholar 

  • Gikas P, Romanos P (2006) Effects of tri-valent (Cr(III)) and hexa-valent (Cr(VI)) chromium on the growth of activated sludge. J Hazard Mater 133(1–3):212–217. doi:10.1016/j.jhazmat.2005.10.023

    Article  PubMed  CAS  Google Scholar 

  • Gikas P, Sengor SS, Ginn T, Moberly J, Peyton B (2009) The effects of heavy metals and temperature on microbial growth and lag. Global Nest J11(3):325–332

    Google Scholar 

  • Grady CPL, Smets BF, Barbeau DS (1996) Variability in kinetic parameter estimates: a review of possible causes and a proposed terminology. Water Res 30(3):742–748. doi:10.1016/0043-1354(95)00199-9

    Article  CAS  Google Scholar 

  • Gutierrez M, Etxebarria J, de las Fuentes L (2002) Evaluation of wastewater toxicity: comparative study between Microtox (R) and activated sludge oxygen uptake inhibition. Water Res 36(4):919–924. doi:10.1016/s0043-1354(01)00299-8

    Article  PubMed  CAS  Google Scholar 

  • Hu ZQ, Chandran K, Grasso D, Smets BF (2002) Effect of nickel and cadmium speciation on nitrification inhibition. Environ Sci Technol 36(14):3074–3078. doi:10.1021/es015784a

    Article  PubMed  CAS  Google Scholar 

  • Insel G, Karahan O, Ozdemir S, Pala L, Katipoglu T, Cokgor EU, Orhon D (2006) Unified basis for the respirometric evaluation of inhibition for activated sludge. J Environ Sci Health A Tox Hazard Subst Environ Eng 41(9):1763–1780. doi:10.1080/10934520600778895

    Article  PubMed  CAS  Google Scholar 

  • ISO 8192 (1995) Water quality—test for inhibition of oxygen consumption by activated sludge

  • Katsou E, Malamis S, Loizidou M (2011) Performance of a membrane bioreactor used for the treatment of wastewater contaminated with heavy metals. Bioresour Technol 102(6):4325–4332. doi:10.1016/j.biortech.2010.10.118

    Article  PubMed  CAS  Google Scholar 

  • Kelly CJ, Tumsaroj N, Lajoie CA (2004) Assessing wastewater metal toxicity with bacterial bioluminescence in a bench-scale wastewater treatment system. Water Res 38(2):423–431. doi:10.1016/s0043-1354(03)00432-9

    Article  PubMed  CAS  Google Scholar 

  • Kong Z, Vanrolleghem P, Verstraete W (1994) Automated respiration inhibition-kinetics analysis (ARIKA) with a respirographic biosensor. Water Sci Technol 30(4):275–284

    CAS  Google Scholar 

  • Kong Z, Vanrolleghem P, Willems P, Verstraete W (1996) Simultaneous determination of inhibition kinetics of carbon oxidation and nitrification with a respirometer. Water Res 30(4):825–836. doi:10.1016/0043-1354(95)00232-4

    Article  CAS  Google Scholar 

  • Madoni P, Romeo MG (2006) Acute toxicity of heavy metals towards freshwater ciliated protists. Environ Pollut 141(1):1–7. doi:10.1016/j.envpol.2005.08.025

    Article  PubMed  CAS  Google Scholar 

  • Malachowska-Jutsz A, Matyja K, Ziembinska A (2011) Cadmium and copper toxicity assessment in activated sludge using ttc bioassay. Arch Environ Prot 37(4):85–94

    CAS  Google Scholar 

  • Malamis S, Katsou E, Daskalakis N, Haralambous KJ (2012) Investigation of the inhibitory effects of heavy metals on heterotrophic biomass activity and their mitigation through the use of natural minerals. J Environ Sci Health A Tox Hazard Subst Environ Eng 47(13):1992–1999. doi:10.1080/10934529.2012.695266

    Article  PubMed  CAS  Google Scholar 

  • Moo-Young M, Blanch HW (1981) Design of biochemical reactors: mass transfer criteria for simple and complex systems. Adv Biochem Eng 19:1–69

    CAS  Google Scholar 

  • Munz G, Gori R, Cammilli L, Lubello C (2008) Characterization of tannery wastewater and biomass in a membrane bioreactor using respirometric analysis. Bioresour Technol 99(18):8612–8618. doi:10.1016/j.biortech.2008.04.004

    Article  PubMed  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51(6):730–750

    Article  PubMed  CAS  Google Scholar 

  • Ochoa-Herrera V, Leon G, Banihani Q, Field JA, Sierra-Alvarez R (2011) Toxicity of copper(II) ions to microorganisms in biological wastewater treatment systems. Sci Total Environ 412:380–385. doi:10.1016/j.scitotenv.2011.09.072

    Article  PubMed  Google Scholar 

  • Oliveira CS, Ordaz A, Ferreira EC, Alves M, Thalasso F (2011) In situ pulse respirometric methods for the estimation of kinetic and stoichiometric parameters in aerobic microbial communities. Biochem Eng J 58–59:12–19. doi:10.1016/j.bej.2011.08.001

    Article  Google Scholar 

  • Ong SA, Toorisaka E, Hirata M, Hano T (2005) The behavior of Ni(II), Cr(III), and Zn(II) in biological wastewater treatment process. Acta Hydroch Hydrob 33(2):95–103. doi:10.1002/aheh.200400559

    Article  Google Scholar 

  • Ordaz A, Oliveira CS, Alba J, Carrion M, Thalasso F (2011) Determination of apparent kinetic and stoichiometric parameters in a nitrifying fixed-bed reactor by in situ pulse respirometry. Biochem Eng J 55(2):123–130. doi:10.1016/j.bej.2011.03.015

    Article  CAS  Google Scholar 

  • Ordaz A, Oliveira CS, Quijano G, Ferreira EC, Alves M, Thalasso F (2012) Kinetic and stoichiometric characterization of a fixed biofilm reactor by pulse respirometry. J Biotechnol 157(1):173–179. doi:10.1016/j.jbiotec.2011.10.015

    Article  PubMed  CAS  Google Scholar 

  • Ozbelge TA, Ozbelge HO, Altinten P (2007) Effect of acclimatization of microorganisms to heavy metals on the performance of activated sludge process. J Hazard Mater 142(1–2):332–339. doi:10.1016/j.jhazmat.2006.08.031

    Article  PubMed  Google Scholar 

  • Pacheco A, Hernandez-Mireles I, Garcia-Martinez C, Alvarez MM (2013) Microplates as a microreactor platform for microalgae research. Biotechnol Prog 29(3):638–644. doi:10.1002/btpr.1721

    Article  PubMed  CAS  Google Scholar 

  • Pai TY, Wang SC, Lo HM, Chiang CF, Liu MH, Chiou RJ, Chen WY, Hung PS, Liao WC, Leu HG (2009) Novel modeling concept for evaluating the effects of cadmium and copper on heterotrophic growth and lysis rates in activated sludge process. J Hazard Mater 166(1):200–206. doi:10.1016/j.jhazmat.2008.11.009

    Article  PubMed  CAS  Google Scholar 

  • Pamukoglu MY, Kargi F (2007) Mathematical modeling of copper(II) ion inhibition on COD removal in an activated sludge unit. J Hazard Mater 146(1–2):372–377. doi:10.1016/j.jhazmat.2006.12.033

    Article  PubMed  CAS  Google Scholar 

  • Polo AM, Tobajas M, Sanchis S, Mohedano AF, Rodriguez JJ (2011) Comparison of experimental methods for determination of toxicity and biodegradability of xenobiotic compounds. Biodegradation 22(4):751–761. doi:10.1007/s10532-010-9448-7

    Article  PubMed  CAS  Google Scholar 

  • Puigdomenech I (2001) HYDRA MEDUSA: make equilibrium diagrams using sophisticated algorithms. KTH Royal Institute of Technology, Stockholm

    Google Scholar 

  • Ramirez-Vargas R, Ordaz A, Carrion M, Hernandez-Paniagua IY, Thalasso F (2013) Comparison of static and dynamic respirometry for the determination of stoichiometric and kinetic parameters of a nitrifying process. Biodegradation 24(5):675–684. doi:10.1007/s10532-012-9615-0

    Article  PubMed  CAS  Google Scholar 

  • Rathnayake IVN, Megharaj M, Krishnamurti GSR, Bolan NS, Naidu R (2013) Heavy metal toxicity to bacteria—are the existing growth media accurate enough to determine heavy metal toxicity? Chemosphere 90(3):1195–1200. doi:10.1016/j.chemosphere.2012.09.036

    Article  PubMed  CAS  Google Scholar 

  • Sciban M, Radetic B, Kevresan D, Klasnja M (2007) Adsorption of heavy metals from electroplating wastewater by wood sawdust. Bioresour Technol 98(2):402–409. doi:10.1016/j.biortech.2005.12.014

    Article  PubMed  CAS  Google Scholar 

  • Smolyakov BS, Ryzhikh AP, Bortnikova SB, Saeva OP, Chernova NY (2010) Behavior of metals (Cu, Zn and Cd) in the initial stage of water system contamination: effect of pH and suspended particles. Appl Geochem 25(8):1153–1161. doi:10.1016/j.apgeochem.2010.05.001

    Article  CAS  Google Scholar 

  • Spanjers H, Takacs I, Brouwer H (1999) Direct parameter extraction from respirograms for wastewater and biomass characterization. Water Sci Technol 39(4):137–145. doi:10.1016/s0273-1223(99)00068-2

    Article  Google Scholar 

  • Stasinakis AS, Thomaidis NS, Giannes AS, Lekkas TD (2003) Effect of arsenic and mercury speciation on inhibition of respiration rate in activated sludge systems. Environ Sci Pollut Res 10(3):177–182. doi:10.1065/espr2002.05.121

    Article  CAS  Google Scholar 

  • Ustun GE (2009) Occurrence and removal of metals in urban wastewater treatment plants. J Hazard Mater 172(2–3):833–838. doi:10.1016/j.jhazmat.2009.07.073

    Article  PubMed  Google Scholar 

  • Utgikar VP, Chaudhary N, Koeniger A, Tabak HH, Haines JR, Govind R (2004) Toxicity of metals and metal mixtures: analysis of concentration and time dependence for zinc and copper. Water Res 38(17):3651–3658. doi:10.1016/j.watres.2004.05.022

    Article  PubMed  CAS  Google Scholar 

  • Van Nostrand JD, Sowder AG, Bertsch PM, Morris PJ (2005) Effect of pH on the toxicity of nickel and other divalent metals to Burkholderia cepacia Pr1(301). Environ Toxicol Chem 24(11):2742–2750

    Article  PubMed  Google Scholar 

  • Vankova S, Kupec J, Hoffmann J (1999) Toxicity of chromium to activated sludge. Ecotoxicol Environ Saf 42(1):16–21

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Hu X, Chen ML, Wu YH (2005) Total concentrations and fractions of Cd, Cr, Pb, Cu, Ni and Zn in sewage sludge from municipal and industrial wastewater treatment plants. J Hazard Mater 119(1–3):245–249. doi:10.1016/j.jhazmat.2004.11

    Article  PubMed  CAS  Google Scholar 

  • Wang X-H, Gai L-H, Sun X-F, Xie H-J, Gao M-M, Wang S-G (2010) Effects of long-term addition of Cu(II) and Ni(II) on the biochemical properties of aerobic granules in sequencing batch reactors. Appl Microbiol Biotechnol 86(6):1967–1975. doi:10.1007/s00253-010-2467-9

    Article  PubMed  CAS  Google Scholar 

  • Wong KY, Zhang MQ, Li XM, Lo WH (1997) A luminescence-based scanning respirometer for heavy metal toxicity monitoring. Biosens Bioelectron 12(2):125–133. doi:10.1016/s0956-5663(97)87058-3

    Article  CAS  Google Scholar 

  • Zhou X-H, Yu T, Shi H-C, Shi H-M (2011) Temporal and spatial inhibitory effects of zinc and copper on wastewater biofilms from oxygen concentration profiles determined by microelectrodes. Water Res 45(2):953–959. doi:10.1016/j.watres.2010.09.035

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by “Consejo Nacional de Ciencia y Tecnología” (project 133338). We also gratefully acknowledge the “Consejo Nacional de Ciencia y Tecnología” for the financial support to Ivonne Esquivel-Rios (Grant # 225319). The authors are thankful to Victoria T. Velázquez-Martínez, Juan Corona-Hernández and Joel Alba-Flores for their technical assistance. The authors declare no conflict of interest.

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  1. Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), Departamento de Biotecnología y Bioingeniería, Av. IPN 2508 San Pedro Zacatenco, 07360, Mexico City, Mexico

    Ivonne Esquivel-Rios & Frederic Thalasso

  2. Departamento de Química, Unidad Iztapalapa, Universidad Autónoma Metropolitana, San Rafael Atlixco No. 186, Col. Vicentina, Iztapalapa, 09340, Mexico City, Mexico

    Ignacio González

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  1. Ivonne Esquivel-Rios
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  2. Ignacio González
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  3. Frederic Thalasso
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Correspondence to Frederic Thalasso.

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Esquivel-Rios, I., González, I. & Thalasso, F. Microrespirometric characterization of activated sludge inhibition by copper and zinc. Biodegradation 25, 867–879 (2014). https://doi.org/10.1007/s10532-014-9706-1

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