Advertisement

Applied Microbiology and Biotechnology

, Volume 99, Issue 1, pp 55–66 | Cite as

Biofilm dynamics characterization using a novel DO-MEA sensor: mass transport and biokinetics

  • Xavier Guimerà
  • Ana Moya
  • Antonio David Dorado
  • Rosa Villa
  • David Gabriel
  • Gemma Gabriel
  • Xavier Gamisans
Environmental biotechnology

Abstract

Biodegradation process modeling is an essential tool for the optimization of biotechnologies related to gaseous pollutant treatment. In these technologies, the predominant role of biofilm, particularly under conditions of no mass transfer limitations, results in a need to determine what processes are occurring within the same. By measuring the interior of the biofilms, an increased knowledge of mass transport and biodegradation processes may be attained. This information is useful in order to develop more reliable models that take biofilm heterogeneity into account. In this study, a new methodology, based on a novel dissolved oxygen (DO) and mass transport microelectronic array (MEA) sensor, is presented in order to characterize a biofilm. Utilizing the MEA sensor, designed to obtain DO and diffusivity profiles with a single measurement, it was possible to obtain distributions of oxygen diffusivity and biokinetic parameters along a biofilm grown in a flat plate bioreactor (FPB). The results obtained for oxygen diffusivity, estimated from oxygenation profiles and direct measurements, revealed that changes in its distribution were reduced when increasing the liquid flow rate. It was also possible to observe the effect of biofilm heterogeneity through biokinetic parameters, estimated using the DO profiles. Biokinetic parameters, including maximum specific growth rate, the Monod half-saturation coefficient of oxygen, and the maintenance coefficient for oxygen which showed a marked variation across the biofilm, suggest that a tool that considers the heterogeneity of biofilms is essential for the optimization of biotechnologies.

Keywords

Heterotrophic biofilm Dissolved oxygen Biofilm profiling MEA sensor Effective diffusivity Biokinetic parameters 

Notes

Acknowledgments

This work has been founded by projects DPI2011-28262-C04 and CTM2012-37927-C03/FEDER, financed by the Ministerio de Economía y Competitividad (Spain). Ana Moya gratefully acknowledges an FPI-2012 predoctoral scholarship, and Xavier Guimerà also acknowledges an FPI-UPC predoctoral scholarship, both from Ministerio de Economía y Competitividad (Spain).

References

  1. (1998) APHA Standard methods for the examination of water and wastewater, Edition 20Google Scholar
  2. Berg P, Risgaard-Petersen N, Silkeborg D (1998) Interpretation of measured concentration profiles in sediment pore water-PI. 1500–1510Google Scholar
  3. Beuling EE, van Den Heuvel JC, Ottengraf SP (2000) Diffusion coefficients of metabolites in active biofilms. Biotechnol Bioeng 67:53–60PubMedCrossRefGoogle Scholar
  4. Beyenal H (2000) Combined effect of substrate concentration and flow velocity on effective diffusivity in biofilms. Water Res 34:528–538. doi: 10.1016/S0043-1354(99)00147-5 CrossRefGoogle Scholar
  5. Beyenal H, Lewandowski Z (2002) Internal and external mass transfer in biofilms grown at various flow velocities. 55–61Google Scholar
  6. Beyenal H, Tanyolaç A, Lewandowski Z (1998) Measurement of local effective diffusivity in heterogeneous biofilm. Water Sci Technol 38:171–178CrossRefGoogle Scholar
  7. Bishop P, Zhang T, Fu Y (1995) Effects of biofilm structure, microbial distributions and mass transport on biodegradation processes. Water Sci Technol 31:143–152CrossRefGoogle Scholar
  8. Bonilla D, Mallén M, de la Rica R, Fernández-Sánchez C, Baldi A (2011) Electrical readout of protein microarrays on regular glass slides. Anal Chem 83:1726–1731. doi: 10.1021/ac102938z PubMedCrossRefGoogle Scholar
  9. Brouwer H, Klapwijk A, Keesman KJ (1998) Identification of activated sludge and wastewater characteristics using respirometric batch-experiments. Water Res 32:1240–1254. doi: 10.1016/S0043-1354(97)00334-5 CrossRefGoogle Scholar
  10. Chiu ZC, Chen MY, Lee DJ, Tay ST, Tay JH, Show KY (2006) Diffusivity of oxygen in aerobic granules. doi:  10.1002/bit
  11. Dawson DA, Trass O (1972) Mass transfer at rough surfaces. Int J Heat Mass Transf 15:1317–1336CrossRefGoogle Scholar
  12. Del Campo FJ, Ordeig O, Vigués N, Godino N, Mas J, Muñoz FX (2007) Continuous measurement of acute toxicity in water using a solid state microrespirometer. Sensors Actuators B Chem 126:515–521. doi: 10.1016/j.snb.2007.03.038 CrossRefGoogle Scholar
  13. Del Campo FJ, Abad L, Illa X, Prats-Alfonso E, Borrisé X, Cirera JM, Bai H-Y, Tsai Y-C (2014) Determination of heterogeneous electron transfer rate constants at interdigitated nanoband electrodes fabricated by an optical mix-and-match process. Sensors Actuators B Chem 194:86–95. doi: 10.1016/j.snb.2013.12.016 CrossRefGoogle Scholar
  14. Dorado AD, Baquerizo G, Maestre JP, Gamisans X, Gabriel D, Lafuente J (2008) Modeling of a bacterial and fungal biofilter applied to toluene abatement: kinetic parameters estimation and model validation. Chem Eng J 140:52–61. doi: 10.1016/j.cej.2007.09.004 CrossRefGoogle Scholar
  15. Dorado AD, Baeza JA, Lafuente J, Gabriel D, Gamisans X (2012) Biomass accumulation in a biofilter treating toluene at high loads—part 1: experimental performance from inoculation to clogging. Chem Eng J 209:661–669. doi: 10.1016/j.cej.2012.08.018 CrossRefGoogle Scholar
  16. Fischer LM, Tenje M, Heiskanen AR, Masuda N, Castillo J, Bentien A, Émneus J, Jakobsen MH, Boisen A (2009) Gold cleaning methods for electrochemical detection applications. Microelectron Eng 86:1282–1285. doi: 10.1016/j.mee.2008.11.045 CrossRefGoogle Scholar
  17. Fu YC, Zhang TC, Bishop PL (1994) Determination of effective oxygen diffusivity in biofilms grown in a completely mixed biodrum reactor. Water Sci. Technol. Pergamon Press Inc, pp 455–462Google Scholar
  18. Gabriel G, Erill I, Caro J, Gómez R, Riera D, Villa R, Godignon P (2007) Manufacturing and full characterization of silicon carbide-based multi-sensor micro-probes for biomedical applications. Microelectron J 38:406–415. doi: 10.1016/j.mejo.2006.11.008 CrossRefGoogle Scholar
  19. Gao X, Lee J, White HS (1995) Natural convection at microelectrodes. Anal Chem 67:1541–1545. doi: 10.1021/ac00105a011 CrossRefGoogle Scholar
  20. Godino N, Dávila D, Vigués N, Ordeig O, del Campo FJ, Mas J, Muñoz FX (2008) Measuring acute toxicity using a solid-state microrespirometer. Sensors Actuators B Chem 135:13–20. doi: 10.1016/j.snb.2008.06.056 CrossRefGoogle Scholar
  21. Guimera A, Gabriel G, Plata-Cordero M, Montero L, Maldonado MJ, Villa R (2012) A non-invasive method for an in vivo assessment of corneal epithelium permeability through tetrapolar impedance measurements. Biosens Bioelectron 31:55–61. doi: 10.1016/j.bios.2011.09.039 PubMedCrossRefGoogle Scholar
  22. Guimerà A, Illa X, Traver E, Plata-Cordero M, Yeste J, Herrero C, Lagunas C, Maldonado MJ, Villa R (2013) Flexible probe for in vivo quantification of corneal epithelium permeability through non-invasive tetrapolar impedance measurements. Biomed Microdevices 15:849–858. doi: 10.1007/s10544-013-9772-x PubMedCrossRefGoogle Scholar
  23. Hibiya K, Nagai J, Tsuneda S, Hirata A (2004) Simple prediction of oxygen penetration depth in biofilms for wastewater treatment. Biochem Eng J 19:61–68. doi: 10.1016/j.bej.2003.10.003 CrossRefGoogle Scholar
  24. Hille A, Neu TR, Hempel DC, Horn H (2009) Effective diffusivities and mass fluxes in fungal biopellets. Biotechnol Bioeng 103:1202–1213. doi: 10.1002/bit.22351 PubMedCrossRefGoogle Scholar
  25. Kim S, Deshusses MA (2003) Development and experimental validation of a conceptual model for biotrickling filtration of H2S. 119–128Google Scholar
  26. La Rosa CD, Yu T (2006) Development of an automation system to evaluate the three-dimensional oxygen distribution in wastewater biofilms using microsensors. Sensors Actuators B Chem 113:47–54. doi: 10.1016/j.snb.2005.02.025 CrossRefGoogle Scholar
  27. Lee J-H, Lim T-S, Seo Y, Bishop PL, Papautsky I (2007) Needle-type dissolved oxygen microelectrode array sensors for in situ measurements. Sensors Actuators B Chem 128:179–185. doi: 10.1016/j.snb.2007.06.008 CrossRefGoogle Scholar
  28. Lewandowski Z, Beyenal H (2007) Fundamentals of biofilm research. 452Google Scholar
  29. Liu S, Chen Y (2009) Measurement of dissolved oxygen and its diffusivity in aerobic granules using a microelectrode array. Environ Sci Technol 43:1160–1165PubMedCrossRefGoogle Scholar
  30. Melo LF, Frias RR (2004) Biofilm physical structure, internal diffusivity and tortuosity. Water Sci Technol 52:77–84Google Scholar
  31. Mitchell DA, von Meien OF, Krieger N, Dalsenter FDH (2004) A review of recent developments in modeling of microbial growth kinetics and intraparticle phenomena in solid-state fermentation. Biochem Eng J 17:15–26. doi: 10.1016/S1369-703X(03)00120-7 CrossRefGoogle Scholar
  32. Mottola HA (1978) Enzymic substrate determination in closed flow-through systems by sample injection and amperometric monitoring of dissolved oxygen levels. Anal Chem 50:94–98CrossRefGoogle Scholar
  33. Ning Y-F, Chen Y-P, Li S, Guo J-S, Gao X, Fang F, Shen Y, Zhang K (2012) Development of an in situ dissolved oxygen measurement system and calculation of its effective diffusion coefficient in a biofilm. Anal Methods 4:2242. doi: 10.1039/c2ay25132a CrossRefGoogle Scholar
  34. Okabe S, Itoh T, Satoh H, Watanabe Y (1999) Analyses of spatial distributions of sulfate-reducing bacteria and their activity in aerobic wastewater biofilms. Appl Environ Microbiol 65:5107–5116PubMedCentralPubMedGoogle Scholar
  35. Paliteiro C (1994) (100)-Type behaviour of polycrystalline gold towards O2 reduction. Electrochim Acta 39:1633–1639CrossRefGoogle Scholar
  36. Perry RH, Green DW (1997) Perry’s chemical engineer’s handbook, 7th edition. Mc Graw-HillGoogle Scholar
  37. Picioreanu C, van Loosdrecht MC, Heijnen JJ (1998) Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol Bioeng 58:101–116PubMedCrossRefGoogle Scholar
  38. Prehn R, Abad L, Sánchez-Molas D, Duch M, Sabaté N, del Campo FJ, Muñoz FX, Compton RG (2011) Microfabrication and characterization of cylinder micropillar array electrodes. J Electroanal Chem 662:361–370. doi: 10.1016/j.jelechem.2011.09.002 CrossRefGoogle Scholar
  39. Rasmussen K, Lewandowski Z (1998) Microelectrode measurements of local mass transport rates in heterogeneous biofilms. Biotechnol Bioeng 59:302–309PubMedCrossRefGoogle Scholar
  40. Revsbech N, Jørgensen B (1986) Microelectrodes: their use in microbial ecology. Adv Microb Ecol 9:293–352CrossRefGoogle Scholar
  41. Revsbech NP, Nielsen LP, Ramsing NB (1998) A novel microsensor for determination of apparent diffusivity in sediments. Limnol Oceanogr 43:986–992CrossRefGoogle Scholar
  42. Schramm A, Larsen LH, Revsbech NP, Ramsing NB, Amann R, Schleifer KH (1996) Structure and function of a nitrifying biofilm as determined by in situ hybridization and the use of microelectrodes. Appl Environ Microbiol 62:4641–4647PubMedCentralPubMedGoogle Scholar
  43. Schwermer CU, Lavik G, Abed RMM, Dunsmore B, Ferdelman TG, Stoodley P, Gieseke A, de Beer D (2008) Impact of nitrate on the structure and function of bacterial biofilm communities in pipelines used for injection of seawater into oil fields. Appl Environ Microbiol 74:2841–2851. doi: 10.1128/AEM.02027-07 PubMedCentralPubMedCrossRefGoogle Scholar
  44. Wu C-C, Yasukawa T, Shiku H, Matsue T (2005) Fabrication of miniature Clark oxygen sensor integrated with microstructure. Sensors Actuators B Chem 110:342–349. doi: 10.1016/j.snb.2005.02.014 CrossRefGoogle Scholar
  45. Yang S, Lewandowski Z (1995) Measurement of local mass transfer coefficient in biofilms. Biotechnol Bioeng 48:737–744. doi: 10.1002/bit.260480623 PubMedCrossRefGoogle Scholar
  46. Yurt N, Sears J, Lewandowski Z (2002) Multiple substrate growth kinetics of Leptothrix discophora SP-6. Biotechnol Prog 18:994–1002. doi: 10.1021/bp0255098 PubMedCrossRefGoogle Scholar
  47. Yurt N, Beyenal H, Sears J, Lewandowski Z (2003) Quantifying selected growth parameters of Leptothrix discophora SP-6 in biofilms from oxygen concentration profiles. Chem Eng Sci 58:4557–4566. doi: 10.1016/S0009-2509(03)00344-0 CrossRefGoogle Scholar
  48. Zhang TC, Bishop PL (1994) Density, porosity, and pore structure of biofilms. Water Res 28:2267–2277. doi: 10.1016/0043-1354(94)90042-6 CrossRefGoogle Scholar
  49. Zhou X-H, Liu J, Song H-M, Qiu Y-Q, Shi H-C (2012) Estimation of heterotrophic biokinetic parameters in wastewater biofilms from oxygen concentration profiles by microelectrode. Environ Eng Sci 29:466–471. doi: 10.1089/ees.2010.0456 CrossRefGoogle Scholar
  50. Zhu X, Suidan MT, Alonso C, Yu T, Kim BJ, Kim BR (2001) Biofilm structure and mass transfer in a gas phase trickle-bed biofilter. Water Sci Technol 43:285–293PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Xavier Guimerà
    • 1
  • Ana Moya
    • 2
    • 3
  • Antonio David Dorado
    • 1
  • Rosa Villa
    • 2
    • 3
  • David Gabriel
    • 4
  • Gemma Gabriel
    • 2
    • 3
  • Xavier Gamisans
    • 1
  1. 1.Department of Mining Engineering and Natural ResourcesUniversitat Politècnica de CatalunyaManresaSpain
  2. 2.Instituto de Microelectrónica de Barcelona, IMB-CNM (CSIC), Esfera UABCampus Universitat Autònoma de BarcelonaBellaterraSpain
  3. 3.Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (CIBER-BBN)ZaragozaSpain
  4. 4.Department of Chemical EngineeringUniversitat Autònoma de BarcelonaBellaterraSpain

Personalised recommendations