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Improving Substrate Consumption and Decrease of Growth Yield in Aerobic Cultures of Pseudomonas denitrificans By Applying Low Voltages in Bioelectric Systems

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Abstract

It is well known that activated sludge treatment systems generate a lot of surplus sludge having environmental and economic impacts. Although several approaches have been proposed for the treatment/reuse of the excess of sludge, there are few studies focused on decreasing the biomass yield without affecting the metabolic activity. This work reports the effect of low magnitude electrical fields (0.07 to 0.2 V/cm) on the growth yield of a pure strain of Pseudomonas denitrificans (used as model microorganism). Cell potentials between 0.2 and 0.57 V were measured during 24 h to the aerobic culture; biomass production and substrate consumption were evaluated at regular intervals. Results indicated that the substrate (lactate) consumption efficiency increased with the applied potential, up to 100%, while the yield diminished 31% (0.34 g biomass/g lactate consumed) at 0.7 V vs. NHE. Bioenergetics showed that the fraction of electron equivalents toward biomass synthesis decreased from 0.68 (when no potential was applied) to 0.47 at 0.57 V, pointing out the redirection of the energy flow toward maintenance to cope with the stress caused by the imposed voltage. Therefore, the electrical stimulus could be used as control of biomass growth in aerobic wastewater treatment lines.

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  • 06 December 2019

    The original version of this article unfortunately contained a mistake in Equation 1.

References

  1. Liu, Y. (2003). Chemically reduced excess sludge production in the activated sludge process. Chemosphere, 50(1), 1–7. https://doi.org/10.1016/S0045-6535(02)00551-9.

    Article  CAS  PubMed  Google Scholar 

  2. Liu, Y., & Tay, J. H. (2001). Strategy for minimization of excess sludge production from the activated sludge process. Biotechnology Advances, 19(2), 97–107. https://doi.org/10.1016/S0734-9750(00)00066-5.

    Article  PubMed  Google Scholar 

  3. Pan, S. C., & Tseng, D. H. (2001). Sewage sludge ash characteristics and its potential applications. Water Science and Technology, 44(10), 261–267. https://doi.org/10.2166/wst.2001.0636.

    Article  CAS  PubMed  Google Scholar 

  4. Stolarek, P., & Ledakowicz, S. (2001). Thermal processing of sewage sludge by drying, pyrolysis, gasification and combustion. Water Science and Technology, 44(10), 333–340. https://doi.org/10.2166/wst.2001.0636.

    Article  CAS  PubMed  Google Scholar 

  5. Guo, W. Q., Yang, S. S., Xiang, W. S., Wang, X. J., & Ren, N. Q. (2013). Minimization of excess sludge production by in-situ activated sludge treatment processes - A comprehensive review. Biotechnology Advances, 31(8), 1386–1396. https://doi.org/10.1016/j.biotechadv.2013.06.003.

    Article  CAS  PubMed  Google Scholar 

  6. Wang, Q., Wei, W., Gong, Y., Yu, Q., Li, Q., Sun, J., & Yuan, Z. (2017). Technologies for reducing sludge production in wastewater treatment plants: State of the art. Science of the Total Environment, 587-588, 510–521. https://doi.org/10.1016/j.scitotenv.2017.02.203.

    Article  CAS  PubMed  Google Scholar 

  7. Ray, S., & Peters, C. A. (2008). Changes in microbiological metabolism under chemical stress. Chemosphere, 71(3), 474–483. https://doi.org/10.1016/j.chemosphere.2007.10.026.

    Article  CAS  PubMed  Google Scholar 

  8. Schimel, J., Balser, T. S., & Wallenstein, M. (2007). Microbial stress-response physiology and its implications. Ecology, 88(6), 1386–1394. https://doi.org/10.1890/06-021.

    Article  PubMed  Google Scholar 

  9. Schröder, U., Harnisch, F., & Angenent, L. T. (2015). Microbial electrochemistry and technology: Terminology and classification. Energy and Environmental Science, 8(2), 513–519. https://doi.org/10.1039/c4ee03359k.

    Article  Google Scholar 

  10. Thrash, J. C., & Coates, J. D. (2008). Review : Direct and indirect electrical stimulation of microbial metabolism. Environmental Science and Technology, 42(11), 3921–3931. https://doi.org/10.1021/es702668w.

    Article  CAS  PubMed  Google Scholar 

  11. Fleming, J. T. (2010). Electronic interfacing with living cells. Advances in Biochemical Engineering / Biotechnology, 117, 155–178. https://doi.org/10.1007/BFb0103032.

    Article  CAS  PubMed  Google Scholar 

  12. Bajracharya, S., Sharma, M., Mohanakrishna, G., Dominguez Benneton, X., Strik, D. P. B. T. B., Sarma, P. M., & Pant, D. (2016). An overview on emerging bioelectrochemical systems (BESs): Technology for sustainable electricity, waste remediation, resource recovery, chemical production and beyond. Renewable Energy, 98, 153–170. https://doi.org/10.1016/j.renene.2016.03.002.

    Article  CAS  Google Scholar 

  13. Velasco-Alvarez, N., González, I., Damian-Matsumura, P., & Gutiérrez-Rojas, M. (2011). Enhanced hexadecane degradation and low biomass production by Aspergillus niger exposed to an electric current in a model system. Bioresource Technology, 102(2), 1509–1515. https://doi.org/10.1016/j.biortech.2010.07.111.

    Article  CAS  PubMed  Google Scholar 

  14. Parvanova-Mancheva, T., & Beschkov, V. (2009). Microbial denitrification by immobilized bacteria Pseudomonas denitrificans stimulated by constant electric field. Biochemical Engineering Journal, 44(2–3), 208–213. https://doi.org/10.1016/j.bej.2008.12.005.

    Article  CAS  Google Scholar 

  15. Beschkov, V., Velizarov, S., Agathos, S. N., & Lukova, V. (2004). Bacterial denitrification of waste water stimulated by constant electric field. Biochemical Engineering Journal, 17(2), 141–145. https://doi.org/10.1016/S1369-703X(03)00149-9.

    Article  CAS  Google Scholar 

  16. Thrash, J. C., Van Trump, J. I., Weber, K. A., Miller, E., Achenbach, L. A., & Coates, J. D. (2007). Electrochemical stimulation of microbial perchlorate reduction. Environmental Science and Technology, 41(5), 1740–1746. https://doi.org/10.1021/es062772m.

    Article  CAS  PubMed  Google Scholar 

  17. Yin, X., Qiao, S., & Zhou, J. (2015). Using electric field to enhance the activity of Anammox bacteria. Applied Microbiology and Biotechnology, 99(16), 6921–6930. https://doi.org/10.1007/s00253-015-6631-0.

    Article  CAS  PubMed  Google Scholar 

  18. Rittmann, B. E., & McCarty, P. L. (2000). Environmental biotechnology: Principles and applications (First ed.). Boston: McGraw-Hill.

    Google Scholar 

  19. APHA/AWWA/WEF. (2012). Standard methods for the examination of water and wastewater. Standard Methods, 541 ISBN 9780875532356.

  20. Soga, T., & Ross, G. A. (1999). Simultaneous determination of inorganic anions, organic acids and metal cations by capillary electrophoresis. Journal of Chromatography A, 834(1–2), 65–71. https://doi.org/10.1016/S0021-9673(98)00692-X.

    Article  CAS  Google Scholar 

  21. Guo, K., Soeriyadi, A. H., Feng, H., Prévoteau, A., Patil, S. A., Gooding, J. J., & Rabaey, K. (2015). Heat-treated stainless steel felt as scalable anode material for bioelectrochemical systems. Bioresource Technology, 195, 46–50. https://doi.org/10.1016/j.biortech.2015.06.060.

    Article  CAS  PubMed  Google Scholar 

  22. Cantu, J. C., Tarango, M., Beier, H. T., & Ibey, B. L. (2016). The biological response of cells to nanosecond pulsed electric fields is dependent on plasma membrane cholesterol. Biochimica et Biophysica Acta - Biomembranes, 1858(11), 2636–2646. https://doi.org/10.1016/j.bbamem.2016.07.006.

    Article  CAS  Google Scholar 

  23. Ibey, B. L., Xiao, S., Schoenbach, K. H., Murphy, M. R., & Pakhomov, A. G. (2009). Plasma membrane permeabilization by 60- and 600-ns electric pulses is determined by the absorbed dose. Bioelectromagnetics, 30(2), 92–99. https://doi.org/10.1002/bem.20451.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Dehghani, S., Rezaee, A., & Hosseinkhani, S. (2018). Effect of alternating electrical current on denitrifying bacteria in a microbial electrochemical system: biofilm viability and ATP assessment. Environmental Science and Pollution Research, 25(33), 33591–33598. https://doi.org/10.1007/s11356-018-3170-0.

    Article  CAS  PubMed  Google Scholar 

  25. Qiao, S., Yin, X., Zhou, J., & Furukawa, K. (2014). Inhibition and recovery of continuous electric field application on the activity of Anammox biomass. Biodegradation, 25(4), 505–513. https://doi.org/10.1007/s10532-013-9677-7.

    Article  PubMed  Google Scholar 

  26. Shin, H., Zeikus, J., & Jain, M. (2002). Electrically enhanced ethanol fermentation by Clostridium thermocellum and Saccharomyces cerevisiae. Applied Microbiology and Biotechnology, 58(4), 476–481. https://doi.org/10.1007/s00253-001-0923-2.

    Article  CAS  PubMed  Google Scholar 

  27. Baudler, A., Schmidt, I., Langner, M., Greiner, A., & Schröder, U. (2015). Does it have to be carbon? Metal anodes in microbial fuel cells and related bioelectrochemical systems. Energy and Environmental Science, 8(7), 2048–2055. https://doi.org/10.1039/c5ee00866b.

    Article  CAS  Google Scholar 

  28. Valle, A., Zanardini, E., Abbruscato, P., Argenzio, P., Lustrato, G., Ranalli, G., & Sorlini, C. (2007). Effects of low electric current (LEC) treatment on pure bacterial cultures. Journal of Applied Microbiology, 103(5), 1376–1385. https://doi.org/10.1111/j.1365-2672.2007.03374.x.

    Article  CAS  PubMed  Google Scholar 

  29. Kumar, Y., Kumar Patel, K., & Kumar, V. (2015). Pulsed electric field processing in food technology. International Journal of Engineering Studies and Technical Approach, 1(2), 6–17 ISSN 2395-0900.

    Google Scholar 

  30. Smith, K. C., Son, R. S., Gowrishankar, T. R., & Weaver, J. C. (2014). Emergence of a large pore subpopulation during electroporating pulses. Bioelectrochemistry, 100, 3–10. https://doi.org/10.1016/j.bioelechem.2013.10.009.

    Article  CAS  PubMed  Google Scholar 

  31. Van Loey, A., Verachtert, B., & Hendrickx, M. (2002). Effects of high electric field pulses on enzymes. Trends in Food Science & Technology, 12, 94–102. https://doi.org/10.1016/S0924-2244(01)00066-8.

    Article  Google Scholar 

  32. Aragón, C., Quiroga, J. M., & Coello, M. D. (2009). Comparison of four chemical uncouplers for excess sludge reduction. Environmental Technology, 30(7), 707–714. https://doi.org/10.1080/09593330902894372.

    Article  CAS  PubMed  Google Scholar 

  33. Gostomski, P. A., & De Vela, R. J. (2018). Metabolic uncouplers for controlling biomass accumulation in biological waste treatment systems. Reviews in Environmental Science and Biotechnology, 17(1), 1–18. https://doi.org/10.1007/s11157-017-9452-z.

    Article  Google Scholar 

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Acknowledgments

The authors acknowledge the technical assistance of Elizabeth Cortés and Guillermo Vidriales. Y. Toriz acknowledges the scholarship provided by CONACYT to perform master studies. We also thank Alessandro Carmona for useful comments.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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Authors and Affiliations

  1. División de Ciencias Ambientales, Instituto Potosino de Investigación Científica y Tecnológica, Camino a la Presa San José 2055, Lomas 4a. Sección, San Luis Potosí, S.L.P, C.P.78216, México, Mexico

    Luis F. Cházaro-Ruiz, María Irene López-Cázares, Yanet Toriz, Felipe Alatriste-Mondragon, Marcela Santana & Lourdes B. Celis

  2. Departamento de Química, Universidad Autónoma Metropolitana – Iztapalapa, Apdo. Postal 55-534, 09340, México City, 09340, Mexico

    Ignacio González

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  1. Luis F. Cházaro-Ruiz
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Cházaro-Ruiz, L.F., López-Cázares, M.I., González, I. et al. Improving Substrate Consumption and Decrease of Growth Yield in Aerobic Cultures of Pseudomonas denitrificans By Applying Low Voltages in Bioelectric Systems. Appl Biochem Biotechnol 190, 1333–1348 (2020). https://doi.org/10.1007/s12010-019-03168-x

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