Empirical Evidence and Mathematical Modelling of Carbamazepine Degradative Kinetics by a Wood-Rotting Microbial Consortium

Waste and Biomass Valorization volume 12, pages995–1003(2021)Cite this article

Abstract

An experimental evolution system with a wood-rotting microbial consortium (BOS08) has demonstrated the acquisition of a new ability to exploit a previously untapped carbon source, such as the recalcitrant carbamazepine (CBZ). The improved extraction method has provided an accurate CBZ depletion rate from BOS08 of \(2.14 \pm 0.42 \times 10^{-3}\;\text{ h }^{-1}\). The consortium did not use cometabolism to process CBZ and the intermediate metabolite produced 10,11-dihydroxycarbamazepine was not pharmacologically active and toxic. The bacteria identification by massive sequencing (Illumina) confirmed the dominance of Proteobacteria Phylum such as genera Cupriavidus sp., Sphingomonas sp., Delftia sp., Acinetobacter sp. and Methylobacterium sp. coexisting through all biodegradation process. Based on biological principles, we model the consortium-CBZ kinetics with a set of nonlinear ordinary differential equations with logistic growth type terms. The use of experimental data combined with logistic growth models allow us to test new functional features acquired by the consortium.

Graphic Abstract

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Jarvis, A.L., Bernot, M.J., Bernot, R.J.: The effects of the psychiatric drug carbamazepine on freshwater invertebrate communities and ecosystem dynamics. Sci. Total Environ. 496, 461 (2014). https://doi.org/10.1016/j.scitotenv.2014.07.084

    Article  Google Scholar 

  2. 2.

    Quinn, B., Schmidt, W., O’Rourke, K., Hernan, R.: Effects of the pharmaceuticals gemfibrozil and diclofenac on biomarker expression in the zebra mussel (Dreissena polymorpha) and their comparison with standardised toxicity tests. Chemosphere 84(5), 657 (2011). https://doi.org/10.1016/j.chemosphere.2011.03.033

    Article  Google Scholar 

  3. 3.

    Ellis, J.: Pharmaceutical and personal care products (PPCPs) in urban receiving waters. Environ. Pollut. 144(1), 184 (2006). https://doi.org/10.1016/j.envpol.2005.12.018. Soil and Sediment Remediation (SSR)

    Article  Google Scholar 

  4. 4.

    Bendz, D., Paxéus, N.A., Ginn, T.R., Loge, F.J.: Occurrence and fate of pharmaceutically active compounds in the environment, a case study: Höje River in Sweden. J. Hazard. Mater. 122(3), 195 (2005). https://doi.org/10.1016/j.jhazmat.2005.03.012. Pharmaceuticals in the Environment

    Article  Google Scholar 

  5. 5.

    Grossberger, A., Hadar, Y., Borch, T., Chefetz, B.: Biodegradability of pharmaceutical compounds in agricultural soils irrigated with treated wastewater. Environ. Pollut. 185, 168 (2014). https://doi.org/10.1016/j.envpol.2013.10.038

    Article  Google Scholar 

  6. 6.

    Benotti, M.J., Trenholm, R.A., Vanderford, B.J., Holady, J.C., Stanford, B.D., Snyder, S.A.: Pharmaceuticals and endocrine disrupting compounds in U.S. drinking water. Environ. Sci. Technol. 43(3), 597 (2009). https://doi.org/10.1021/es801845a

    Article  Google Scholar 

  7. 7.

    Norvill, Z.N., Shilton, A., Guieysse, B.: Emerging contaminant degradation and removal in algal wastewater treatment ponds: identifying the research gaps. J. Hazard. Mater. 313, 291 (2016)

    Article  Google Scholar 

  8. 8.

    González Alonso, S., Catalá, M., Maroto, R.R., Gil, J.L.R., de Miguel, A.G., Valcárcel, Y.: Pollution by psychoactive pharmaceuticals in the Rivers of Madrid metropolitan area (Spain). Environ. Int. 36(2), 195 (2010). https://doi.org/10.1016/j.envint.2009.11.004

    Article  Google Scholar 

  9. 9.

    Lin, B., Lyu, J., jin Lyu, X., Yu, H qing, Hu, Z., Lam, J.C., Lam, P.K.: Characterization of cefalexin degradation capabilities of two Pseudomonas strains isolated from activated sludge. J. Hazard. Mater. 282, 158 (2015). https://doi.org/10.1016/j.jhazmat.2014.06.080. Advances in Analysis, Treatment Technologies, and Environmental Fate of Emerging Contaminants

    Article  Google Scholar 

  10. 10.

    Patel, M., Kumar, R., Kishor, K., Mlsna, T., Pittman, C.U., Mohan, D.: Pharmaceuticals of emerging concern in aquatic systems: chemistry, occurrence, effects, and removal methods. Chem. Rev. 119(6), 3510 (2019). https://doi.org/10.1021/acs.chemrev.8b00299

    Article  Google Scholar 

  11. 11.

    Thelusmond, J.R., Strathmann, T.J., Cupples, A.M.: The identification of carbamazepine biodegrading phylotypes and phylotypes sensitive to carbamazepine exposure in two soil microbial communities. Sci. Total Environ. 571, 1241 (2016). https://doi.org/10.1016/j.scitotenv.2016.07.154

    Article  Google Scholar 

  12. 12.

    Zhang, Y., Geißen, S.U., Gal, C.: Carbamazepine and diclofenac: removal in wastewater treatment plants and occurrence in water bodies. Chemosphere 73(8), 1151 (2008). https://doi.org/10.1016/j.chemosphere.2008.07.086

    Article  Google Scholar 

  13. 13.

    Brozinski, J.M., Lahti, M., Meierjohann, A., Oikari, A., Kronberg, L.: The anti-inflammatory drugs diclofenac, naproxen and ibuprofen are found in the bile of wild fish caught downstream of a wastewater treatment plant. Environ. Sci. Technol. 47(1), 342 (2013). https://doi.org/10.1021/es303013j. PMID: 23186122

    Article  Google Scholar 

  14. 14.

    Luo, Y., Guo, W., Ngo, H.H., Nghiem, L.D., Hai, F.I., Zhang, J., Liang, S., Wang, X.C.: A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci. Total Environ. 473–474, 619 (2014). https://doi.org/10.1016/j.scitotenv.2013.12.065

    Article  Google Scholar 

  15. 15.

    Wang, J., Wang, S.: Removal of pharmaceuticals and personal care products (PPCPs) from wastewater: a review. J. Environ. Manag. 182, 620 (2016). https://doi.org/10.1016/j.jenvman.2016.07.049

    Article  Google Scholar 

  16. 16.

    García-Espinoza, J.D., Mijaylova-Nacheva, P., Avilés-Flores, M.: Electrochemical carbamazepine degradation: effect of the generated active chlorine, transformation pathways and toxicity. Chemosphere 192, 142 (2018). https://doi.org/10.1016/j.chemosphere.2017.10.147

    Article  Google Scholar 

  17. 17.

    Rao, Y., Yang, H., Xue, D., Guo, Y., Qi, F., Ma, J.: Sonolytic and sonophotolytic degradation of Carbamazepine: kinetic and mechanisms. Ultrason. Sonochem. 32, 371 (2016). https://doi.org/10.1016/j.ultsonch.2016.04.005

    Article  Google Scholar 

  18. 18.

    Tiwari, B., Sellamuthu, B., Ouarda, Y., Drogui, P., Tyagi, R.D., Buelna, G.: Review on fate and mechanism of removal of pharmaceutical pollutants from wastewater using biological approach. Bioresour. Technol. 224, 1 (2017). https://doi.org/10.1016/j.biortech.2016.11.042

    Article  Google Scholar 

  19. 19.

    Chen, X., Vollertsen, J., Nielsen, J.L., Gieraltowska Dall, A., Bester, K.: Degradation of PPCPs in activated sludge from different WWTPs in Denmark. Ecotoxicology 24(10), 2073 (2015). https://doi.org/10.1007/s10646-015-1548-z

    Article  Google Scholar 

  20. 20.

    Deng, Y., Li, B., Yu, K., Zhang, T.: Biotransformation and adsorption of pharmaceutical and personal care products by activated sludge after correcting matrix effects. Sci. Total Environ. 544, 980 (2016). https://doi.org/10.1016/j.scitotenv.2015.12.010

    Article  Google Scholar 

  21. 21.

    de Voogt, P., Janex-Habibi, M.L., Sacher, F., Puijker, L., Mons, M.: Development of a common priority list of pharmaceuticals relevant for the water cycle. Water Sci. Technol. 59(1), 39 (2009). https://doi.org/10.2166/wst.2009.764

    Article  Google Scholar 

  22. 22.

    Martin Ruel, S., Choubert, J.M., Budzinski, H., Miége, C., Esperanza, M., Coquery, M.: Occurrence and fate of relevant substances in wastewater treatment plants regarding Water Framework Directive and future legislations. Water Sci. Technol. 65(7), 1179 (2012). https://doi.org/10.2166/wst.2012.943

    Article  Google Scholar 

  23. 23.

    Xiong, J.Q., Kurade, M.B., Abou-Shanab, R.A., Ji, M.K., Choi, J., Kim, J.O., Jeon, B.H.: Biodegradation of carbamazepine using freshwater microalgae Chlamydomonas mexicana and Scenedesmus obliquus and the determination of its metabolic fate. Bioresour. Technol. 205, 183 (2016). https://doi.org/10.1016/j.biortech.2016.01.038

    Article  Google Scholar 

  24. 24.

    Bessa, V., Moreira, I., Tiritan, M., Castro, P.: Enrichment of bacterial strains for the biodegradation of diclofenac and carbamazepine from activated sludge. Int. Biodeterior. Biodegrad. 120, 135 (2017). https://doi.org/10.1016/j.ibiod.2017.02.008

    Article  Google Scholar 

  25. 25.

    Hata, T., Shintate, H., Kawai, S., Okamura, H., Nishida, T.: Elimination of carbamazepine by repeated treatment with laccase in the presence of 1-hydroxybenzotriazole. J. Hazard. Mater. 181(1–3), 1175 (2010)

    Article  Google Scholar 

  26. 26.

    Zhang, Y., Geissen, S.U.: Elimination of carbamazepine in a non-sterile fungal bioreactor. Bioresour. Technol. 112, 221 (2012). https://doi.org/10.1016/j.biortech.2012.02.073

    Article  Google Scholar 

  27. 27.

    Golan-Rozen, N., Seiwert, B., Riemenschneider, C., Reemtsma, T., Chefetz, B., Hadar, Y.: Transformation pathways of the recalcitrant pharmaceutical compound carbamazepine by the white-rot fungus Pleurotus ostreatus: effects of growth conditions. Environ. Sci. Technol. 49(20), 12351 (2015)

    Article  Google Scholar 

  28. 28.

    Rodarte-Morales, A.I., Feijoo, G., Moreira, M.T., Lema, J.M.: Degradation of selected pharmaceutical and personal care products (PPCPs) by white-rot fungi. World J. Microbiol. Biotechnol. 27(8), 1839 (2011). https://doi.org/10.1007/s11274-010-0642-x

    Article  Google Scholar 

  29. 29.

    Rodríguez-Rodríguez, C.E., Marco-Urrea, E., Caminal, G.: Degradation of naproxen and carbamazepine in spiked sludge by slurry and solid-phase Trametes versicolor systems. Bioresour. Technol. 101(7), 2259 (2010). https://doi.org/10.1016/j.biortech.2009.11.089

    Article  Google Scholar 

  30. 30.

    Simarro, R., González, N., Bautista, L.F., Molina, M.C.: Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by a wood-degrading consortium at low temperatures. FEMS Microbiol. Ecol. 83(2), 438 (2013). https://doi.org/10.1111/1574-6941.12006

    Article  Google Scholar 

  31. 31.

    Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Lozupone, C.A., Turnbaugh, P.J., Fierer, N., Knight, R.: Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Nat. Acad. Sci. USA 108(Supplement 1), 4516 (2011). https://doi.org/10.1073/pnas.1000080107

    Article  Google Scholar 

  32. 32.

    Jelic, A., Cruz-Morató, C., Marco-Urrea, E., Sarrà, M., Perez, S., Vicent, T., Petrović, M., Barcelo, D.: Degradation of carbamazepine by Trametes versicolor in an air pulsed fluidized bed bioreactor and identification of intermediates. Water Res. 46(4), 955 (2012). https://doi.org/10.1016/j.watres.2011.11.063

    Article  Google Scholar 

  33. 33.

    Swinnen, I.A.M., Bernaerts, K., Dens, E.J., Geeraerd, A.H., Van Impe, J.F.: Predictive modelling of the microbial lag phase: a review. Int. J. Food Microbiol. 94(2), 137 (2004). https://doi.org/10.1016/j.ijfoodmicro.2004.01.006

    Article  Google Scholar 

  34. 34.

    Munoz-Lopez, M., Edwards, M., Schumann, Uea: Multiplicative modelling of four-phase microbial growth. Pac. J. Math. Ind. 7(7), 1 (2015). https://doi.org/10.1186/s40736-015-0018-0

    MathSciNet  Article  MATH  Google Scholar 

  35. 35.

    Li, A., Cai, R., Cui, D., Qiu, T., Pang, C., Yang, J., Ma, F., Ren, N.: Characterization and biodegradation kinetics of a new cold-adapted carbamazepine-degrading bacterium, Pseudomonas sp. CBZ-4. J. Environ. Sci. 25(11), 2281 (2013). https://doi.org/10.1016/S1001-0742(12)60293-9

    Article  Google Scholar 

  36. 36.

    Monod, J.: Recherches Sur La Croissance Des Cultures Bacteriennes. Hermann & cie, Paris (1942)

    Google Scholar 

  37. 37.

    Kunze, H., Vrscay, E.: Solving inverse problems for ordinary differential equations using the Picard contraction mapping. Inverse Prob. 15, 745 (1999)

    MathSciNet  Article  Google Scholar 

  38. 38.

    Yuan, X., Li, S., Hu, J., Yu, M., Li, Y., Wang, Z.: Experiments and numerical simulation on the degradation processes of carbamazepine and triclosan in surface water: a case study for the Shahe Stream, South China. Sci. Total Environ. 655, 1125 (2019)

    Article  Google Scholar 

  39. 39.

    Ungureanu, C.P., Favier, L., Bahrim, G., Amrane, A.: Response surface optimization of experimental conditions for carbamazepine biodegradation by Streptomyces MIUG 4.89. New Biotechnol. 32(3), 347 (2015). https://doi.org/10.1016/j.nbt.2014.12.005

    Article  Google Scholar 

  40. 40.

    Zhou, J., Yu, X., Ding, C., Wang, Z., Zhou, Q., Pao, H., Cai, W.: Optimization of phenol degradation by Candida tropicalis Z-04 using Plackett-Burman design and response surface methodology. J. Environ. Sci. 23(1), 22 (2011). https://doi.org/10.1016/S1001-0742(10)60369-5

    Article  Google Scholar 

  41. 41.

    Pfeiffer, T., Bonhoeffer, S.: Evolution of cross-feeding in microbial populations. Am. Nat. 163(6), E126 (2004). https://doi.org/10.1086/383593

    Article  Google Scholar 

  42. 42.

    Barrick, J.E., Yu, D.S., Yoon, S.H., Jeong, H., Oh, T.K., Lenski, D.S.R.E., Kim, J.F.: Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243 (2009)

    Article  Google Scholar 

  43. 43.

    de Gonzalo, G., Colpa, D.I., Habib, M.H., Fraaije, M.W.: Bacterial enzymes involved in lignin degradation. J. Biotechnol. 236, 110 (2016). https://doi.org/10.1016/j.jbiotec.2016.08.011

    Article  Google Scholar 

  44. 44.

    Woo, H.L., Hazen, T.C., Simmons, B.A., DeAngelis, K.M.: Enzyme activities of aerobic lignocellulolytic bacteria isolated from wet tropical forest soils. Syst. Appl. Microbiol. 37(1), 60 (2014). https://doi.org/10.1016/j.syapm.2013.10.001

    Article  Google Scholar 

  45. 45.

    Bugg, T.D., Ahmad, M., Hardiman, E.M., Singh, R.: The emerging role for bacteria in lignin degradation and bio-product formation. Curr. Opin. Biotechnol. 22(3), 394 (2011). https://doi.org/10.1016/j.copbio.2010.10.009. Energy biotechnology - Environmental biotechnology

    Article  Google Scholar 

  46. 46.

    Popa, C., Favier, L., Dinica, R., Semrany, S., Djelal, H., Amrane, A., Bahrim, G.: Potential of newly isolated wild Streptomyces strains as agents for the biodegradation of a recalcitrant pharmaceutical, carbamazepine. Environ. Technol. 35(24), 3082 (2014). https://doi.org/10.1080/09593330.2014.931468. PMID: 25244136

    Article  Google Scholar 

  47. 47.

    Kolter, R., Siegele, D.A., Tormo, A.: The stationary phase of the bacterial life cycle. Annu. Rev. Microbiol. 47(1), 855 (1993)

    Article  Google Scholar 

  48. 48.

    Lazazzera, B.A.: Quorum sensing and starvation: signals for entry into stationary phase. Curr. Opin. Microbiol. 3(2), 177 (2000). https://doi.org/10.1016/S1369-5274(00)00072-2

    Article  Google Scholar 

  49. 49.

    Tormo, A., Navarro Llorens, J.M., Martínez-García, E.: Stationary phase in gram-negative bacteria. FEMS Microbiol. Rev. 34(4), 476 (2010). https://doi.org/10.1111/j.1574-6976.2010.00213.x

    Article  Google Scholar 

  50. 50.

    Goo, E., An, J.H., Kang, Y., Hwang, I.: Control of bacterial metabolism by quorum sensing. Trends Microbiol. 23(9), 567 (2015). https://doi.org/10.1016/j.tim.2015.05.007

    Article  Google Scholar 

  51. 51.

    Suutari, M., Lignell, U., Hyvärinen, A., Nevalainen, A.: Media for cultivation of indoor streptomycetes. J. Microbiol. Methods 51(3), 411 (2002). https://doi.org/10.1016/S0167-7012(02)00100-8

    Article  Google Scholar 

  52. 52.

    Miao, X.S., Yang, J.J., Metcalfe, C.D.: Carbamazepine and its metabolites in wastewater and in biosolids in a municipal wastewater treatment plant. Environ. Sci. Technol. 39(19), 7469 (2005)

    Article  Google Scholar 

  53. 53.

    Klampfl, C.W.: Metabolization of pharmaceuticals by plants after uptake from water and soil: a review. Trends Anal. Chem. 111, 13 (2019). https://doi.org/10.1016/j.trac.2018.11.042

    Article  Google Scholar 

  54. 54.

    Sauvêtre, A., May, R., Harpaintner, R., Poschenrieder, C., Schröder, P.: Metabolism of carbamazepine in plant roots and endophytic rhizobacteria isolated from Phragmites australis. J. Hazard. Mater. 342, 85 (2018). https://doi.org/10.1016/j.jhazmat.2017.08.006

    Article  Google Scholar 

  55. 55.

    Miao, X.S., Metcalfe, C.D.: Determination of carbamazepine and its metabolites in aqueous samples using liquid chromatography electrospray tandem mass spectrometry. Anal. Chem. 75(15), 3731 (2003). https://doi.org/10.1021/ac030082k

    Article  Google Scholar 

  56. 56.

    Aubenneau, M., Tahar, A., Casellas, C., Wisniewski, C.: Membrane bioreactor for pharmaceutically active compounds removal: effects of carbamazepine on mixed microbial communities implied in the treatment. Process Biochem. 45(11), 1826 (2010). https://doi.org/10.1016/j.procbio.2010.04.011. Bioprocess Engineering - SFGP2009

    Article  Google Scholar 

  57. 57.

    Bray, S.R., Kitajima, K., Mack, M.C.: emporal dynamics of microbial communities on decomposing leaf litter of 10 plant species in relation to decomposition rate. Soil Biol. Biochem. 49, 30 (2012). https://doi.org/10.1016/j.soilbio.2012.02.009

    Article  Google Scholar 

  58. 58.

    Soares, M., Rousk, J.: Microbial growth and carbon use efficiency in soil: links to fungal-bacterial dominance, SOC-quality and stoichiometry. Soil Biol. Biochem. 131, 195 (2019). https://doi.org/10.1016/j.soilbio.2019.01.010

    Article  Google Scholar 

  59. 59.

    Thelusmond, J.R., Strathmann, T.J., Cupples, A.M.: Carbamazepine, triclocarban and triclosan biodegradation and the phylotypes and functional genes associated with xenobiotic degradation in four agricultural soils. Sci. Total Environ. 657, 1138 (2019). https://doi.org/10.1016/j.scitotenv.2018.12.145

    Article  Google Scholar 

  60. 60.

    Kraigher, B., Kosjek, T., Heath, E., Kompare, B., Mandic-Mulec, I.: Influence of pharmaceutical residues on the structure of activated sludge bacterial communities in wastewater treatment bioreactors. Water Res. 42(17), 4578 (2008). https://doi.org/10.1016/j.watres.2008.08.006

    Article  Google Scholar 

  61. 61.

    Ramírez-Durán, N., Moreno-Pérez, P.A., Sandoval-Trujillo, A.H.: Ecopharmacovigilance (Springer), chap. Bacterial Treatment of Pharmaceutical Industry Effluents., p. chap. 19 (2017)

  62. 62.

    Chopra, D., Kumar, S.: Advances in animal biotechnology and its applications (Springer, Singapore), chap. Pharmaceuticals and Personal Care Products (PPCPs) as Emerging Environmental Pollutants: Toxicity and Risk Assessment., pp. 337–353 (2018)

  63. 63.

    Camargo-Neves, A.A., Araújo, W.L.: In: Shukla, P. Applied Microbiology and Bioengineering. Academic Press, pp. 87–99. (2019) https://doi.org/10.1016/B978-0-12-815407-6.00006-X

Download references

Acknowledgements

M. Arrayás is supported by the research grant from the Spanish Ministry of Economy and Competitiveness ESP2017-86263-C4-3-R.

Author information

Affiliations

  1. Departamento de Biología y Geología, Física y Química Inorgánica, Universidad Rey Juan Carlos, Tulipán s/n, 28933, Móstoles, Madrid, Spain

    N. González-Benítez & M. C. Molina

  2. Área de Electromagnetismo, Universidad Rey Juan Carlos, Tulipán s/n, 28933, Móstoles, Madrid, Spain

    M. Arrayás

Authors
  1. N. González-Benítez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. C. Molina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Arrayás
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. González-Benítez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

González-Benítez, N., Molina, M.C. & Arrayás, M. Empirical Evidence and Mathematical Modelling of Carbamazepine Degradative Kinetics by a Wood-Rotting Microbial Consortium. Waste Biomass Valor 12, 995–1003 (2021). https://doi.org/10.1007/s12649-020-01041-1

Download citation

Keywords

  • Wood-rotting consortium
  • Carbamazepine
  • Proteobacteria
  • Kinetics modelling