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Evolution of the microbial community of the biofilm in a methane-based membrane biofilm reactor reducing multiple electron acceptors

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Abstract

Previous work documented complete perchlorate reduction in a membrane biofilm reactor (MBfR) using methane as the sole electron donor and carbon source. This work explores how the biofilm’s microbial community evolved as the biofilm stage-wise reduced different combinations of perchlorate, nitrate, and nitrite. The initial inoculum, carrying out anaerobic methane oxidation coupled to denitrification (ANMO-D), was dominated by uncultured Anaerolineaceae and Ferruginibacter sp. The microbial community significantly changed after it was inoculated into the CH4-based MBfR and fed with a medium containing perchlorate and nitrite. Archaea were lost within the first 40 days, and the uncultured Anaerolineaceae and Ferruginibacter sp. also had significant losses. Replacing them were anoxic methanotrophs, especially Methylocystis, which accounted for more than 25 % of total bacteria. Once the methanotrophs became important, methanol-oxidizing denitrifying bacteria, namely, Methloversatilis and Methylophilus, became important in the biofilm, probably by utilizing organic matter generated by the metabolism of methanotrophs. When methane consumption was equal to the maximum-possible electron-donor supply, Methylomonas, also an anoxic methanotroph, accounted for >10 % of total bacteria and remained a major part of the community until the end of the experiments. We propose that aerobic methane oxidation coupled to denitrification and perchlorate reduction (AMO-D and AMO-PR) directly oxidized methane and reduced NO3 − to NO2 − or N2O under anoxic condition, producing organic matter for methanol-assimilating denitrification and perchlorate reduction (MA-D and MA-PR) to reduce NO3 −. Simultaneously, bacteria capable of anaerobic methane oxidation coupled to denitrification and perchlorate reduction (ANMO-D and ANMO-PR) used methane as the electron donor to respire NO3 − or ClO4 − directly.

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Acknowledgments

Authors greatly thank the “National Key Technology R&D Program (2014ZX07101-012),” the “National Natural Science Foundation of China (Grant Nos. 21377109 and 21577123),” and the “National High Technology Research and Development Program of China (2013AA06A205)” for their financial support.

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    Authors and Affiliations

    1. Zhejiang Province Key Laboratory for Water Pollution Control and Environmental Safety, Zhejiang University, Hangzhou, Zhejiang, China

      Ran Chen, Yi-Hao Luo, Jia-Xian Chen, Yin Zhang, Li-Lian Wen, Ping Zheng & He-Ping Zhao

    2. MOE Key Laboratory of Environmental Remediation and Ecosystem Health, Zhejiang University, Hangzhou, China

      Li-Lian Wen, Ping Zheng & He-Ping Zhao

    3. Department of Environmental Engineering, College of Environmental and Resource Science, Zhejiang University, Hangzhou, China

      Li-Lian Wen, Ling-Dong Shi, Ping Zheng & He-Ping Zhao

    4. Department of Civil and Environmental Engineering, FAMU-FSU College of Engineering, Florida State University, Tallahassee, FL, 32310-6046, USA

      Youneng Tang

    5. Swette Center for Environmental Biotechnology, Biodesign Institute at Arizona State University, P.O. Box 875701, Tempe, AZ, 85287-5701, USA

      Bruce E. Rittmann

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    1. Ran Chen
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    Correspondence to He-Ping Zhao.

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    Responsible editor: Gerald Thouand

    Ran Chen and Yi-Hao Luo contributed equally to this work.

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    Chen, R., Luo, YH., Chen, JX. et al. Evolution of the microbial community of the biofilm in a methane-based membrane biofilm reactor reducing multiple electron acceptors. Environ Sci Pollut Res 23, 9540–9548 (2016). https://doi.org/10.1007/s11356-016-6146-y

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