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Chlorate addition enhances perchlorate reduction in denitrifying membrane-biofilm reactors

  • Environmental Biotechnology
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Abstract

Perchlorate is a widespread drinking water contaminant with regulatory standards ranging from 2 to 18 μg/L. The hydrogen-based membrane-biofilm reactor (MBfR) can effectively reduce perchlorate, but it is challenging to achieve low-µg/L levels. We explored chlorate addition to increase the abundance of perchlorate-reducing bacteria (PRB) and improve removals. MBfR reactors were operated with and without chlorate addition. Results show that chlorate doubled the abundance of putative PRB (e.g., Rhodocyclales) and improved perchlorate reduction to 23 ± 17 µg/L, compared to 53 ± 37 µg/L in the control. Sulfate reduction was substantially inhibited during chlorate addition, but quickly recovered once suspended. Our results suggest that chlorate addition can enhance perchlorate reduction by providing a selective pressure for PRB. It also decreases net sulfate reduction.

Key points

• Chlorate increased the abundance of perchlorate-reducing bacteria

• Chlorate addition improved perchlorate removal

• Chlorate appeared to suppress sulfate reduction

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • ANSES: French Agency for Food, Environmental and Health Occupational & Safety (2012) ANSES opinion concerning epidemiological studies on associations between exposure to perchlorate in drinking water and thyroid function in specific populations., Vol. 2017. Retrieved 16 May, 2017, from https://www.anses.fr/en/system/files/EAUX2012sa0119EN.pdf

  • Bardiya N, Bae J-H (2011) Dissimilatory perchlorate reduction: a review. Microbiol Res 166(4):237–254

    Article  CAS  Google Scholar 

  • Bomberg M, Lamminmäki T, Itävaara M (2016) Microbial communities and their predicted metabolic characteristics in deep fracture groundwaters of the crystalline bedrock at Olkiluoto, Finland. Biogeosciences 13(21):6031–6047

    Article  CAS  Google Scholar 

  • CA DEPT (California Department of Public Health) (2007) State adoption of a perchlorate standard. Retrieved 16 May, 2017 from: https://www.waterboards.ca.gov/drinking_water/certlic/drinkingwater/documents/perchlorate/AdoptionMemotoWaterSystems-10-2007.pdf

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108(Supplement 1):4516–4522

    Article  CAS  Google Scholar 

  • Carlson HK, Kuehl JV, Hazra AB, Justice NB, Stoeva MK, Sczesnak A, Mullan MR, Iavarone AT, Engelbrektson A, Price MN, Deutschbauer AM, Arkin AP, Coates JD (2015) Mechanisms of direct inhibition of the respiratory sulfate-reduction pathway by (per)chlorate and nitrate. ISME J 9(6):1295–1305

    Article  CAS  Google Scholar 

  • Choe JK, Mehnert MH, Guest JS, Strathmann TJ, Werth CJ (2013) Comparative assessment of the environmental sustainability of existing and emerging perchlorate treatment technologies for drinking water. Environ Sci Technol 47(9):4644–4652

    Article  CAS  Google Scholar 

  • Coates JD, Achenbach LA (2004) Microbial perchlorate reduction: rocket-fuelled metabolism. Nat Rev Microbiol 2(7):569–580

    Article  CAS  Google Scholar 

  • Coates JD, Chakraborty R, Lack JG, O’Connor SM, Cole KA, Bender KS, Achenbach LA (2001) Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411:1039

    Article  CAS  Google Scholar 

  • Coates JD, Michaelidou U, Bruce RA, O’Connor SM, Crespi JN, Achenbach LA (1999) Ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl Environ Microbiol 65(12):5234–5241. https://doi.org/10.1128/AEM.65.12.5234-5241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dasgupta PK, Martinelango PK, Jackson WA, Anderson TA, Tian K, Tock RW, Rajagopalan S (2005) The origin of naturally occurring perchlorate: the role of atmospheric processes. Environ Sci Technol 39(6):1569–1575. https://doi.org/10.1021/es048612x

    Article  CAS  PubMed  Google Scholar 

  • DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a Chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7):5069–5072

    Article  CAS  Google Scholar 

  • EFSA Panel on Contaminants in the Food Chain (EFSA CONTAM Panel) (2014) Scientific opinion on the risks to public health related to the presence of perchlorate in food, in particular fruits and vegetables. EFSA J 12(10):3869

    Article  Google Scholar 

  • Engelbrektson A, Hubbard CG, Tom LM, Boussina A, ** YT, Wong H, Piceno YM, Carlson HK, Conrad ME, Anderson G, Coates JD (2014) Inhibition of microbial sulfate reduction in a flow-through column system by (per)chlorate treatment. Front Microbiol 5:315

    Article  Google Scholar 

  • Engelbrektson AL, Cheng Y, Hubbard CG, ** YT, Arora B, Tom LM, Hu P, Grauel A-L, Conrad ME, Andersen GL, Ajo-Franklin JB, Coates JD (2018) Attenuating sulfidogenesis in a soured continuous flow column system with perchlorate treatment. Front Microbiol 9:1575–1575

    Article  Google Scholar 

  • Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes: Volume 5: Proteobacteria: alpha and beta subclasses. Springer, New York, pp 3–37

    Google Scholar 

  • Kraft B, Tegetmeyer HE, Meier D, Geelhoed JS, Strous M (2014) Rapid succession of uncultured marine bacterial and archaeal populations in a denitrifying continuous culture. Environ Microbiol 16(10):3275–3286

    Article  CAS  Google Scholar 

  • Li R, Tun HM, Jahan M, Zhang Z, Kumar A, Dilantha Fernando WG, Farenhorst A, Khafipour E (2017) Comparison of DNA-, PMA-, and RNA-based 16S rRNA Illumina sequencing for detection of live bacteria in water. Sci Rep 7(1):5752

    Article  Google Scholar 

  • Liu W, Lian J, Guo J, Zhang C, Guo Y, Niu Y, Duan L (2019) Perchlorate reduction by anaerobic granular sludge under different operation strategies: performance, extracellular polymeric substances and microbial community. Bioresour Technol Rep 8:100312. https://doi.org/10.1016/j.biteb.2019.100312

    Article  Google Scholar 

  • Ma H, Bonnie NA, Yu M, Che S, Wang Q (2016) Biological treatment of ammonium perchlorate-contaminated wastewater: a review. J Water Reuse Desalination 7(4):82–107

    Article  Google Scholar 

  • MA DEPT. (Massachussets Department of Environmental Protection) (2006) Update to “Perchlorate Toxicological Profile and Health Assessment”. Available: https://www.mass.gov/doc/310-cmr-2200-the-massachusetts-drinking-water-regulations/download

  • Martin KJ, Nerenberg R (2012) The membrane biofilm reactor (MBfR) for water and wastewater treatment: principles, applications, and recent developments. Bioresour Technol 122:83–94

    Article  CAS  Google Scholar 

  • Martin KJ, Picioreanu C, Nerenberg R (2015) Assessing microbial competition in a hydrogenbased membrane biofilm reactor (MBfR) using multidimensional modeling. Biotechnol Bioeng 112(9):1843–1853. https://doi.org/10.1002/bit.25607

    Article  CAS  PubMed  Google Scholar 

  • Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441

    Article  CAS  Google Scholar 

  • Nerenberg R, Kawagoshi Y, Rittmann BE (2006) Kinetics of a hydrogen-oxidizing, perchlorate-reducing bacterium. Water Res 40(17):3290–3296

    Article  CAS  Google Scholar 

  • Nerenberg R, Kawagoshi Y, Rittmann BE (2008) Microbial ecology of a perchlorate-reducing, hydrogen-based membrane biofilm reactor. Water Res 42(4–5):1151–1159

    Article  CAS  Google Scholar 

  • Ontiveros-Valencia A, Tang Y, Krajmalnik-Brown R, Rittmann BE (2013) Perchlorate reduction from a highly contaminated groundwater in the presence of sulfate-reducing bacteria in a hydrogen-fed biofilm. Biotechnol Bioeng 110(12):3139–3147

    Article  CAS  Google Scholar 

  • Ontiveros-Valencia A, Tang Y, Krajmalnik-Brown R, Rittmann BE (2014a) Managing the interactions between sulfate- and perchlorate-reducing bacteria when using hydrogen-fed biofilms to treat a groundwater with a high perchlorate concentration. Water Res 55:215–224

    Article  CAS  Google Scholar 

  • Ontiveros-Valencia A, Tang Y, Zhao H-P, Friese D, Overstreet R, Smith J, Evans P, Rittmann BE, Krajmalnik-Brown R (2014b) Pyrosequencing analysis yields comprehensive assessment of microbial communities in pilot-scale two-stage membrane biofilm reactors. Environ Sci Technol 48(13):7511–7518

  • Oren A (2014) The Family Xanthobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Berlin Heidelberg, pp 709–726

    Chapter  Google Scholar 

  • Roldán MD, Reyes F, Moreno-Vivián C, Castillo F (1994) Chlorate and nitrate reduction in the phototrophic bacteria Rhodobacter capsulatus and Rhodobacter sphaeroides. Curr Microbiol 29(4):241–245

    Article  Google Scholar 

  • Shao M-F, Zhang T, Fang H (2010) Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications. Appl Microbiol Biotechnol 88:1027–1042

    Article  CAS  Google Scholar 

  • Sijimol MR, Jyothy S, Pradeepkumar AP, Chandran MSS, Ghouse SS, Mohan M (2015) Review on Fate, Toxicity, and Remediation of Perchlorate. Environ Forensics 16(2):125–134

    Article  CAS  Google Scholar 

  • Srinivasan R, Sorial GA (2009) Treatment of perchlorate in drinking water: a critical review. Sep Purif Technol 69(1):7–21

    Article  CAS  Google Scholar 

  • Steinberg LM, Trimble JJ, Logan BE (2005) Enzymes responsible for chlorate reduction by Pseudomonas sp. Are different from those used for perchlorate reduction by Azospira sp. FEMS Microbiol Lett 247(2):153–159. https://doi.org/10.1016/j.femsle.2005.05.003

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Zhao H, Marcus AK, Krajmalnik-Brown R, Rittmann BE (2012) A Steady-State Biofilm Model for Simultaneous Reduction of Nitrate and Perchlorate, Part 2: Parameter Optimization and Results and Discussion. Environ Sci Technol 46(3):1608–1615

    Article  CAS  Google Scholar 

  • Tang Y, Ontiveros-Valencia A, Feng L, Zhou C, Krajmalnik-Brown R, Rittmann BE (2013) A biofilm model to understand the onset of sulfate reduction in denitrifying membrane biofilm reactors. Biotechnol Bioeng 110(3):763–772

    Article  CAS  Google Scholar 

  • US Environmental Protection Agency (US EPA) (2009) Revised Assessment Guidance for Pechlorate. Memorandum to Regional Administrators. US EPA Office of Solid Waste and Emergency Response, Washington, DC

  • Willems A (2014) The Family Comamonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria. Springer, Berlin Heidelberg, pp 777–851

    Chapter  Google Scholar 

  • Willems A., Gillis, M. 2015. Hydrogenophaga. in: Bergey’s manual of systematics of archaea and bacteria, (Ed.) W. B. Whitman, F. Rainey, P. Kämpfer, M. Trujillo, J. Chun, P. DeVos, B. Hedlund and S. Dedysh.

  • World Health Organization (WHO) (2004) Sulfate in drinking-water. WHO Press

    Google Scholar 

  • World Health Organization (WHO) (2011) Nitrate and nitrite in drinking-water. WHO Press

    Google Scholar 

  • World Health Organization (WHO) (2016) Chlorine dioxide, chlorite and chlorate in drinking-water. WHO Press

    Google Scholar 

  • Yang B, Wang Y, Qian P-Y (2016) Sensitivity and correlation of hypervariable regions in 16S rRNA genes in phylogenetic analysis. BMC Bioinformatics 17(1):135. https://doi.org/10.1186/s12859-016-0992-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye L, You H, Yao J, Su H (2012) Water treatment technologies for perchlorate: a review. Desalination 298:1–12

    Article  CAS  Google Scholar 

  • Youngblut MD, Wang O, Barnum TP, Coates JD (2016) (Per)chlorate in biology on Earth and beyond. Annu Rev Microbiol 70:435–457

    Article  CAS  Google Scholar 

  • Zhang S, Pang S, Wang P, Wang C, Guo C, Addo FG, Li Y (2016) Responses of bacterial community structure and denitrifying bacteria in biofilm to submerged macrophytes and nitrate. Sci Rep 6:36178

    Article  CAS  Google Scholar 

  • Zhang M, Li X, Cheng X, Wang X, Song M, Wang X, Ma X (2021) Isotopic tracing of perchlorate sources in the environment. J Chem 2021:9978489. https://doi.org/10.1155/2021/9978489

    Article  CAS  Google Scholar 

  • Zhao HP, Van Ginkel S, Tang Y, Kang DW, Rittmann B, Krajmalnik-Brown R (2011) Interactions between perchlorate and nitrate reductions in the biofilm of a hydrogen-based membrane biofilm reactor. Environ Sci Technol 45(23):10155–10162

    Article  CAS  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge the Center for Environmental Science and Technology (CEST) at Notre Dame for their support with analytical equipment.

Funding

This research was supported by the University of Notre Dame-Pontificia Universidad Católica Collaborative Seed Fund, the CEDEUS (Centro de Desarrollo Urbano Sustentable) CONICYT/FONDAP/15110020, FONDECYT 1201134, and National Scholarship for PhD (CONICYT, Chile) 21161573.

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Authors and Affiliations

  1. Departamento de Ingeniería Hidráulica y Ambiental, Pontificia Universidad Católica de Chile, Av. Vicuña Mackenna 4860, Macul, Santiago, Chile

    Marcela Vega & Ignacio T. Vargas

  2. Department of Civil & Environmental Engineering & Earth Sciences, University of Notre Dame, 156 Fitzpatrick Hall of Engineering, South Bend, IN, 46556, USA

    Marcela Vega, Aura Ontiveros-Valencia & Robert Nerenberg

  3. Centro de Desarrollo Urbano Sustentable (CEDEUS), Av. Vicuña Mackenna 4860, Macul, Santiago, Chile

    Marcela Vega & Ignacio T. Vargas

  4. División de Ciencias Ambientales, Instituto Potosino de Investigación Científica y Tecnológica, Camino a la Presa de San José 2055, CP 78216, San Luis Potosí, México

    Aura Ontiveros-Valencia

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  1. Marcela Vega
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  2. Aura Ontiveros-Valencia
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  3. Ignacio T. Vargas
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  4. Robert Nerenberg
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Contributions

RN, ITV, and MV conceived and designed the research. MV and AOV conducted the experiments and analyzed the data. MV wrote the manuscript. RN, AOV, and ITV revised the manuscript. All authors read and approved the manuscript.

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Correspondence to Robert Nerenberg.

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Vega, M., Ontiveros-Valencia, A., Vargas, I.T. et al. Chlorate addition enhances perchlorate reduction in denitrifying membrane-biofilm reactors. Appl Microbiol Biotechnol 106, 4341–4350 (2022). https://doi.org/10.1007/s00253-022-11976-1

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