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Kinetics of carbendazim degradation in a horizontal tubular biofilm reactor

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Abstract

The fungicide carbendazim is an ecotoxic agent affecting aquatic biota. Due to its suspected hormone-disrupting effects, it is considered a “priority hazard substance” by the Water Framework Directive of the European Commission, and its degradation is of major concern. In this work, a horizontal tubular biofilm reactor (HTBR) operating in plug-flow regime was used to study the kinetics of carbendazim removal by an acclimated microbial consortium. The reactor was operated in steady state continuous culture at eight different carbendazim loading rates. The concentrations of the fungicide were determined at several distances of the HTBR. At the loading rates tested, the highest instantaneous removal rates were observed in the first section of the tubular biofilm reactor. No evidence of inhibition of the catabolic activity of the microbial community was found. Strains of the genera Flectobacillus, Klebsiella, Stenotrophomonas, and Flavobacterium were identified in the biofilm; the last three degrade carbendazim in axenic culture.

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References

  1. Salunkhe VP, Sawant IS, Banerjee K, Wadkar PN, Sawant SD, Hingmire SA (2014) Kinetics of degradation of carbendazim by B. subtilis strains: possibility of in situ detoxification. Environ Monit Assess 186(12):8599–8610. doi:10.1007/s10661-014-4027-8

    Article  CAS  Google Scholar 

  2. Marrs TT, Ballantyne B (2004) Pesticide toxicology and international regulation. Wiley, Hoboken, pp 237–238

    Google Scholar 

  3. Maltby L, Brock TCM, Van den Brink PJ (2009) Fungicide risk assessment for aquatic ecosystems: importance of interspecific variation, toxic mode of action, and exposure regime. Environ Sci Technol 43:7556–7563

    Article  CAS  Google Scholar 

  4. Van den Brick P, Hattink J, Bransen F, Van Donk E (2000) Impact of the fungicide carbendazim in freshwater microcosms II. Zooplankton, primary producers and final conclusions. Aquat Toxicol 48(3):251–264

    Google Scholar 

  5. Nishiuchi Y, Yoshida K (1975) Effects of pesticides on tadpoles. Part 3. Bull Agric Chem Insp Stn (Tokyo) 14:66–68

    Google Scholar 

  6. Kaura T, Toorb AP, Wanchoob RK (2015) Parametric study on degradation of fungicide carbendazim in dilute aqueous solutions using nano TiO2. Desalin Water Treat 54(1):122–131. doi:10.1080/19443994.2013.879081

    Article  Google Scholar 

  7. Govindassamy P, Tiroumavalavane M, Marcelline SO, Ramalingam V (2011) Toxic influence of endocrine disruptor, carbendazim, on brain biochemical and hematological changes in the freshwater fish, Cyprinus carpio. Abstracts of the 47th Congress of the European Societies of Toxicology (EUROTOX). Toxicol Lett 205S:S125. doi:10.1016/j.toxlet.2011.05.447

    Article  Google Scholar 

  8. Macedo E, Bortolan S, Leivas M, Ceccatto DC, Gastaldello E (2014) Reproductive and possible hormonal effects of carbendazim. Regul Toxicol Pharmacol 69:476–486

    Article  Google Scholar 

  9. Andrade TS, Henriques JF, Almeida AR, Machado AL, Koba O, Giang PT, Soares AMVM, Domingues I (2016) Carbendazim exposure induces developmental, biochemical and behavioural disturbance in zebrafish embryos. Aquat Toxicol 170:390–399. doi:10.1016/j.aquatox.2015.11.017

    Article  CAS  Google Scholar 

  10. Environmental Health Criteria 149 (1993) Carbendazim. International Programme on Chemical Safety. World Health Organization, Geneva. http://www.inchem.org/documents/ehc/ehc/ehc149.htm. Consulted 6 Apr 2016

  11. Cuppen JGM, Van den Brink PJ, Camps E, Uil KF, Brock TCM (2000) Impact of the fungicide carbendazim in freshwater microcosms. I. Water quality, breakdown of particulate organic matter and responses of macroinvertebrates. Aquat Toxicol 48:233–250

    Article  CAS  Google Scholar 

  12. Cicek N (2003) A review of membrane bioreactors and their potential application in the treatment of agricultural wastewater. Can Biosyst Eng 45:6.37–6.49

    Google Scholar 

  13. Zhang G-S, Jia X-M, Cheng T-F, Ma X-H, Zhao Y-H (2005) Isolation and characterization of a new carbendazim-degrading Ralstonia sp. strain. World J Microbiol Biotechnol 21(3):265–269. doi:10.1007/s11274-004-3628-8

    Article  Google Scholar 

  14. Xu J, Gu X, Shen B, Wang Z, Wang K, Li S (2006) Isolation and characterization of a carbendazim-degrading Rhodococcus sp. djl-6. Curr Microbiol 53(1):72–76. doi:10.1007/s00284-005-0474-3

    Article  CAS  Google Scholar 

  15. Kalwasińska A, Kesy J, Donderski W, Lalke-Porczyk E (2008) Biodegradation of carbendazim by planktonic and benthic bacteria of eutrophic lake Chełmżyńskie. Pol J Environ Stud 17(4):515–523

    Google Scholar 

  16. Pandey G, Dorrian SJ, Russell RJ, Brearley C, Kotsonis S, Oakeshott JG (2010) Cloning and biochemical characterization of a novel carbendazim (methyl-1 h-benzimidazol-2-ylcarbamate)-hydrolyzing esterase from the newly isolated Nocardioides sp. strain sg-4 g and its potential for use in enzymatic bioremediation. Appl Environ Microbiol 76(9):2940–2945. doi:10.1128/AEM.02990-09

    Article  CAS  Google Scholar 

  17. Feisther VA, Ulson de Souza AA, Trigueros DE, de Mello JM, de Oliveira D, Ulson Guelli, de Souza SM (2015) Biodegradation kinetics of benzene, toluene, and xylene compounds: microbial growth and evaluation of models. Bioprocess Biosyst Eng 38(7):1233–1241. doi:10.1007/s00449-015-1364-0

    Article  CAS  Google Scholar 

  18. Cycoń M, Żmijowska A, Piotrowska-Seget Z (2011) Biodegradation kinetics of 2,4-d by bacterial strains isolated from soil. Cent Eur J Biol 6(2):188–198. doi:10.2478/s11535-011-0005-0

    Google Scholar 

  19. Herrera-Gonzalez VE, Ruiz-Ordaz N, Galindez-Mayer J, Juarez-Ramirez C, Santoyo-Tepole F, Marron Montiel E (2013) Biodegradation of the herbicide propanil, and its 3,4-dichloroaniline by-product in a continuously operated biofilm reactor. World J Microbiol Biotechnol 29(3):467–474. doi:10.1007/s11274-012-1200-5

    Article  CAS  Google Scholar 

  20. Pérez-Bárcena JF, Ahuatzi-Chacón D, Castillo-Martínez KL, Ruiz-Ordaz N, Galíndez-Mayer J, Juárez-Ramírez C, Ramos-Monroy O (2014) Effect of herbicide adjuvants on the biodegradation rate of the methylthiotriazine herbicide prometryn. Biodegradation 25(3):405–415. doi:10.1007/s10532-013-9669-7

    Article  Google Scholar 

  21. Marques R, Oehmen A, Carvalho G, Reis MA (2015) Modelling the biodegradation kinetics of the herbicide propanil and its metabolite 3,4-dichloroaniline. Environ Sci Pollut Res Int 22(9):6687–6695. doi:10.1007/s11356-014-3870-z

    Article  CAS  Google Scholar 

  22. Lawrence AW, McCarty PL (1970) Unified basis for biological treatment design and operation. J Sanit Eng Div 96(3):757–778

    Google Scholar 

  23. Ivancic M, Santek B, Novak S, Horvat P, Maric V (2004) Bioprocess kinetics in a horizontal rotating tubular bioreactor. Bioprocess Biosyst Eng 26:169–175. doi:10.1007/s00449-003-0346-9

    Article  CAS  Google Scholar 

  24. Mann U (2009) Principles of chemical reactor analysis and design: new tools for industrial chemical reactor operations, 2nd edn. Wiley, USA, pp 239–285. doi:10.1002/9780470385821

    Book  Google Scholar 

  25. Pittman RN (2011) Regulation of tissue oxygenation. Chapter 8. matching oxygen supply to oxygen demand. Morgan & Claypool Life Sciences, San Rafael

    Google Scholar 

  26. Taguchi H, Humphrey AE (1966) Dynamic measurement of the volumetric oxygen transfer coefficient in fermentation systems. J Ferment Technol 44:881–889

    CAS  Google Scholar 

  27. Castañón-González JH, Galíndez-Mayer J, Ruiz-Ordaz N, Rocha-Martínez L, Peña-Partida JC, Marrón-Montiel E, Santoyo-Tepole F (2016) Biodegradation of the herbicide Diuron in a packed bed channel and a double biobarrier with distribution of oxygenated liquid by airlift devices: influence of oxygen limitation. New Biotechnol 33(1):7–15. doi:10.1016/j.nbt.2015.07.002

    Article  Google Scholar 

  28. Relman DA (1993) Universal bacterial 16S rRNA amplification and sequencing. In: Persing HD, Smith TF, Tenover CF, White ST (eds) Diagnostic molecular microbiology. Principles and applications. American Chemical Society, Washington, DC, pp 489–495

    Google Scholar 

  29. Hach Company (2014) Water analysis handbook. 9th edn. Colorado, USA. pp 221–224, 399–401

  30. Mazellier P, Leroy E, Legube B (2002) Photochemical behavior of the fungicide carbendazim in dilute aqueous solution. J Photochem Photobiol A Chem 153(1–3):221–227. doi:10.1016/S1010-6030(02)00296-4

    Article  CAS  Google Scholar 

  31. Fang H, Wang Y, Gao C, Yan H, Dong B, Yu Y (2010) Isolation and characterization of Pseudomonas sp. CBW capable of degrading carbendazim. Biodegradation 21(6):939–946. doi:10.1007/s10532-010-9353-0

    Article  CAS  Google Scholar 

  32. Yang C, Hamel C, Vujanovic C, Gan Y (2011) Fungicide: modes of action and possible impact on nontarget microorganisms. ISRN Ecol. doi:10.5402/2011/130289 (Article ID 130289)

    Google Scholar 

  33. Wang X, Song M, Gao C, Dong B, Zhang Q, Fang H, Yu Y (2009) Carbendazim induces a temporary change in soil bacterial community structure. J Environ Sci (China) 21(12):1679–1683. doi:10.1016/S1001-0742(08)62473-0

    Article  CAS  Google Scholar 

  34. Burrows LA, Edwards CA (2004) The use of integrated soil microcosms to assess the impact of carbendazim on soil ecosystems. Ecotoxicol 13(1):143–161. doi:10.1023/B:ECTX.0000012411.14680.21

    Article  CAS  Google Scholar 

  35. Zahran MA, Osman AM, Wahed RA, Attia M, Pedersen EB, Elnasser GA, Turky AS (2015) Design, synthesis and antimicrobial evaluation of novel carbendazim dithioate analogs. Res J Pharm Biol Chem Sci 6(4):1084–1092

    CAS  Google Scholar 

  36. Xiao W, Wang H, Li T, Zhu Z, Zhang J, He Z, Yang X (2013) Bioremediation of Cd and carbendazim co-contaminated soil by Cd-hyperaccumulator Sedum alfredii associated with carbendazim-degrading bacterial strains. Environ Sci Pollut Res 20(1):380–389. doi:10.1007/s11356-012-0902-4

    Article  CAS  Google Scholar 

  37. Sun J, Xu J, Hu H, Hu M (2013) Bacterium for efficiently degrading residual pesticide carbendazim and application thereof. Chinese Patent CN102296041 B

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Acknowledgements

This work was supported by a grant obtained from SIP, Instituto Politécnico Nacional (SIP-IPN 20161072) for N. Ruiz-Ordaz, and (SIP-IPN 20161067) for J. Galíndez-Mayer. The authors wish to thank COFAA-IPN and SNI-Conacyt for fellowships to N. Ruiz-Ordaz, F. Santoyo-Tepole and J. Galindez-Mayer; SNI-Conacyt for fellowships to J. García-Mena; and SIP-IPN for the financial support of ML Alvarado-Gutiérrez.

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Authors and Affiliations

  1. Departamento de Ingeniería, Instituto Politécnico Nacional, ENCB, México, Mexico

    María Luisa Alvarado-Gutiérrez, Nora Ruiz-Ordaz, Juvencio Galíndez-Mayer & Deifilia Ahuatzi-Chacón

  2. Central de Instrumentación de Espectroscopia, Instituto Politécnico Nacional, ENCB, México, Mexico

    Fortunata Santoyo-Tepole

  3. Departamento de Bioquímica, Instituto Politécnico Nacional, ENCB, México, Mexico

    Everardo Curiel-Quesada

  4. Departamento de Genética y Biología Molecular, Cinvestav, Instituto Politécnico Nacional, México, Mexico

    Jaime García-Mena

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  1. María Luisa Alvarado-Gutiérrez
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Correspondence to Nora Ruiz-Ordaz or Juvencio Galíndez-Mayer.

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Alvarado-Gutiérrez, M.L., Ruiz-Ordaz, N., Galíndez-Mayer, J. et al. Kinetics of carbendazim degradation in a horizontal tubular biofilm reactor. Bioprocess Biosyst Eng 40, 519–528 (2017). https://doi.org/10.1007/s00449-016-1717-3

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