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Adaptation of a Methanogenic Consortium to Arsenite Inhibition

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Abstract

Arsenic (As) is a ubiquitous metalloid known for its adverse effects to human health. Microorganisms are also impacted by As toxicity, including methanogenic archaea, which can affect the performance of a process in which biological activity is required (i.e., stabilization of activated sludge in wastewater treatment plants). The novel ability of a mixed methanogenic granular sludge consortium to adapt to the inhibitory effect of arsenic As was investigated by exposing the culture to approximately 0.92 mM of arsenite (AsIII) for 160 days in an arsenate (AsV)-reducing bioreactor using ethanol as the electron donor. The results of shaken batch bioassays indicated that the original, unexposed sludge was severely inhibited by AsIII as evidenced by the low 50 % inhibition concentrations (IC50) determined, i.e., 19 and 90 μM AsIII for acetoclastic and hydrogenotrophic methanogenesis, respectively. The tolerance of the acetoclastic and hydrogenotrophic methanogens in the sludge to AsIII increased 47-fold (IC50 = 910 μM) and 12-fold (IC50 = 1100 μM), respectively, upon long-term exposure to As. In conclusion, the methanogenic community in the granular sludge demonstrated a considerable ability to adapt to the severe inhibitory effects of As after a prolonged exposure period.

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References

  • Ahmann, D., Roberts, A. L., Krumholz, L. R., & Morel, F. M. M. (1994). Microbe grows by reducing arsenic. Nature, 371(6500), 750–750.

    Article  CAS  Google Scholar 

  • APHA. (1999). Standard methods for the examination of water and wastewater. Washington D.C: APHA, AWWA and WEF.

    Google Scholar 

  • ATSDR (2007) Toxicological profile for arsenic. U.S. Department of Health and Human Services, Public Health Service. Atlanta, GA.

  • Bini, E. (2010). Archaeal transformation of metals in the environment. FEMS Microbiology Ecology, 73(1), 1–16.

    CAS  Google Scholar 

  • Cavalca, L., Corsini, A., Zaccheo, P., Andreoni, V., & Muyzer, G. (2013). Microbial transformations of arsenic: perspectives for biological removal of arsenic from water. Future Microbiology, 8(6), 753–768.

    Article  CAS  Google Scholar 

  • Cervantes, C., Ji, G., Ramírez, J. L., & Silver, S. (1994). Resistance to arsenic compounds in microorganisms. FEMS Microbiological Reviews, 15(4), 355–367.

    Article  CAS  Google Scholar 

  • Chen, Y., Cheng, J. J., & Creamer, K. S. (2008). Inhibition of anaerobic digestion process: a review. Bioresource Technology, 99(10), 4044–4064.

    Article  CAS  Google Scholar 

  • Ehrlich, H.L. (2002) Bacterial oxidation of As(III) compounds. Environmental Chemistry of Arsenic. William T. Frankenberger, J. (ed), pp. 313–327, CRC Press, New York, USA.

  • Fernandez, N., Diaz, E. E., Amils, R., & Sanz, J. L. (2008). Analysis of microbial community during biofilm development in an anaerobic wastewater treatment reactor. Microbial Ecology, 56(1), 121–132.

    Article  CAS  Google Scholar 

  • Field, J. A., Sierra-Alvarez, R., Cortinas, I., Feijoo, G., Moreira, M. T., Kopplin, M., & Gandolfi, A. J. (2004). Facile reduction of arsenate in methanogenic sludge. Biodegradation, 15(3), 185–196.

    Article  CAS  Google Scholar 

  • Giller, K. E., Witter, E., & McGrath, S. P. (1998). Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biology and Biochemical, 30(10–11), 1389–1414.

    Article  CAS  Google Scholar 

  • Kruger, M. C., Bertin, P. N., Heipieper, H. J., & Arsene-Ploetze, F. (2013). Bacterial metabolism of environmental arsenic-mechanisms and biotechnological applications. Applied Microbiology Biot, 97(9), 3827–3841.

    Article  CAS  Google Scholar 

  • Li, P., Wang, Y., Jiang, Z., Jiang, H., Li, B., Dong, H., & Wang, Y. (2013). Microbial diversity in high arsenic groundwater in Hetao Basin of Inner Mongolia, China. Geomicrobiol Journal, 30(10), 897–909.

    Article  Google Scholar 

  • Li, A., Luo, J., Xu, W., & Pan, T. (2015). Arsenic removal of high-arsenic wastewater from gallium arsenide semiconductor production by enhanced two-stage treatment. Desalination and Water Treatment, 55(5), 1285–1292.

    CAS  Google Scholar 

  • Mandal, B. K., & Suzuki, K. T. (2002). Arsenic round the world: a review. Talanta, 58(1), 201–235.

    Article  CAS  Google Scholar 

  • O'day, P. A., Vlassopoulos, D., Root, R., & Rivera, N. (2004). The influence of sulfur and iron on dissolved arsenic concentrations in the shallow subsurface under changing redox conditions. Proceedings of the National Academy of Sciences of the United States of America, 101(38), 13703–13708.

    Article  Google Scholar 

  • Oremland, R. S., Hoeft, S. E., Santini, J. A., Bano, N., Hollibaugh, R. A., & Hollibaugh, J. T. (2002). Anaerobic oxidation of arsenite in Mono Lake water and by facultative, arsenite-oxidizing chemoautotroph, strain MLHE-1. Applied and Environmental Microbiology, 68(10), 4795–4802.

    Article  CAS  Google Scholar 

  • Oremland, R. S., Saltikov, C. W., Wolfe-Simon, F., & Stolz, J. F. (2009). Arsenic in the evolution of earth and extraterrestrial ecosystems. Geomicrobiology Journal, 26(7), 522–536.

    Article  CAS  Google Scholar 

  • Paikaray, S. (2015). Arsenic geochemistry of acid mine drainage. Mine Water and the Environment, 34(2), 181–196.

    Article  CAS  Google Scholar 

  • Rodriguez-Freire, L., Sierra-Alvarez, R., Root, R., Chorover, J., & Field, J. A. (2014). Biomineralization of arsenate to arsenic sulfides is greatly enhanced at mildly acidic conditions. Water Research, 66, 242–253.

    Article  CAS  Google Scholar 

  • Rodriguez-Freire, L., Moore, S.E., Sierra-Alvarez, R., Root, R.A., Chorover, J. and Field, J.A. (2015) Arsenic remediation by formation of arsenic sulfide minerals in a continuous anaerobic bioreactor. Biotechnol Bioeng, in press.

  • Rosen, B. P. (2002). Biochemistry of arsenic detoxification. Febs Letter, 529(1), 86–92.

    Article  CAS  Google Scholar 

  • Sierra-Alvarez, R., Cortinas, I., Yenal, U., & Field, J. A. (2004). Methanogenic inhibition by arsenic compounds. Applied and Environmental Microbiology, 70(9), 5688–5691.

    Article  CAS  Google Scholar 

  • Slyemi, D., & Bonnefoy, V. (2012). How prokaryotes deal with arsenic. Environmetal Microbiology Report, 4(6), 571–586.

    CAS  Google Scholar 

  • Tchobanoglous, G., Burton, F. L., Stensel, H. D., & Metcalf and Eddy. (2003). Wastewater engineering: treatment and reuse. Boston, USA: McGraw-Hill Education.

    Google Scholar 

  • Wang, P. P., Sun, G. X., & Zhu, Y. G. (2014). Identification and characterization of arsenite methyltransferase from an archaeon, Methanosarcina acetivorans C2A. Environmental Science and Technology, 48(21), 12706–12713.

    Article  CAS  Google Scholar 

  • Wang, Y. H., Li, P., Dai, X. Y., Zhang, R., Jiang, Z., Jiang, D. W., & Wang, Y. X. (2015). Abundance and diversity of methanogens: potential role in high arsenic groundwater in Hetao Plain of Inner Mongolia, China. Science of the Total Environment, 515–516, 153–161.

    Article  Google Scholar 

  • Yang, H. C., Fu, H. L., Lin, Y. F., & Rosen, B. P. (2012). Pathways of arsenic uptake and efflux. In S. Lutsenko & J. M. Arguello (Eds.), Metal transporters (Current topics in membranes, Vol. 69, pp. 325–358). San Diego: Elsevier Academic Press Inc.

    Chapter  Google Scholar 

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Acknowledgments

This research was funded by a grant of the National Institute of Environment and Health Sciences-supported Superfund Research Program (NIH P42 ES-04940-11). Arsenic speciation analyses were performed by the Arizona Laboratory for Emerging Contaminants (ALEC) at the University of Arizona from our NIEHS-supported Superfund Research Program Grant#2. This work was partially funded by a Water Sustainability Program Fellowship, The University of Arizona, awarded to Lucia Rodriguez-Freire.

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Authors and Affiliations

  1. Department of Chemical and Environmental Engineering, The University of Arizona, P.O. Box 210011, Tucson, AZ, USA

    Lucia Rodriguez-Freire, Sarah E. Moore, Reyes Sierra-Alvarez & James A. Field

Authors
  1. Lucia Rodriguez-Freire
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  2. Sarah E. Moore
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  3. Reyes Sierra-Alvarez
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  4. James A. Field
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Correspondence to Lucia Rodriguez-Freire.

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Rodriguez-Freire, L., Moore, S.E., Sierra-Alvarez, R. et al. Adaptation of a Methanogenic Consortium to Arsenite Inhibition. Water Air Soil Pollut 226, 414 (2015). https://doi.org/10.1007/s11270-015-2672-3

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  • DOI: https://doi.org/10.1007/s11270-015-2672-3

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