SpringerLink
Log in

Response of Propionate-Degrading Methanogenic Microbial Communities to Inhibitory Conditions

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Propionate is a crucial intermediate during methane fermentation. Investigating the effects of different kinds of inhibitors on the propionate-degrading microbial community is necessary to develop countermeasures for improving process stability. In the present study, under inhibitory conditions (acetate, propionate, sulfide, and ammonium addition), the dynamic changes of the propionate-degrading microbial community from a mesophilic chemostat fed with propionate as the sole carbon source were investigated using high-throughput sequencing of 16S rRNA. Sulfide and/or ammonia inhibited specific species in the microbial community. Compared with Syntrophobacter, Smithella was more resistant to inhibition by sulfide and/or ammonia. However, Syntrophobacter demonstrated greater tolerance than Smithella under acid inhibition conditions. Some genera that had close phylogenetic relationships and similar functions showed similar responses to different inhibitors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Lettinga, G. (1995). Anaerobic digestion and wastewater treatment systems. Antonie Van Leeuwenhoek, 67(1), 3–28.

    Article  CAS  PubMed  Google Scholar 

  2. Dupla, M., Conte, T., Bouvier, J. C., Bernet, N., & Steyer, J. P. (2004). Dynamic evaluation of a fixed bed anaerobic digestion process in response to organic overloads and toxicant shock loads. Water Science and Technology, 49(1), 61–68.

    Article  CAS  PubMed  Google Scholar 

  3. Hansen, K. H., Angelidaki, I., & Ahring, B. K. (1998). Anaerobic digestion of swine manure: inhibition by ammonia. Water Research, 32(1), 5–12.

    Article  CAS  Google Scholar 

  4. Lens, P. N. L., Visser, A., Janssen, A. J. H., Pol, L. W. H., & Lettinga, G. (1998). Biotechnological treatment of sulfate-rich wastewaters. Critical Reviews in Environmental Science and Technology, 28(1), 41–88.

    Article  CAS  Google Scholar 

  5. Bouallagui, H., Touhami, Y., Ben Cheikh, R., & Hamdi, M. (2005). Bioreactor performance in anaerobic digestion of fruit and vegetable wastes. Process Biochemistry, 40(3-4), 989–995.

    Article  CAS  Google Scholar 

  6. Sung, S., & Liu, T. (2003). Ammonia inhibition on thermophilic anaerobic digestion. Chemosphere, 53(1), 43–52.

    Article  CAS  PubMed  Google Scholar 

  7. Parkin, G., Speece, R., Yang, C., & Kocher, W. (1983). Response of methane fermentation systems to industrial toxicants. Journal - Water Pollution Control Federation , 55(1), 44–53.

  8. Hill, D. T., Cobb, S. A., & Bolte, J. P. (1987). Using volatile fatty acid relationships to predict anaerobic digester failure. Transactions of ASAE, 30(2), 496–0501.

    Article  CAS  Google Scholar 

  9. Ahring, B. K., Sandberg, M., & Angelidaki, I. (1995). Volatile fatty acids as indicators of process imbalance in anaerobic digestors. Applied Microbiology and Biotechnology, 43(3), 559–565.

    Article  CAS  Google Scholar 

  10. Barredo, M. S., & Evison, L. M. (1991). Effect of propionate toxicity on methanogen-enriched sludge, Methanobrevibacter smithii, and Methanospirillum hungatii at different pH values. Applied and Environmental Microbiology, 57(6), 1764–1769.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Briones, A., & Raskin, L. (2003). Diversity and dynamics of microbial communities in engineered environments and their implications for process stability. Current Opinion in Biotechnology, 14(3), 270–276.

    Article  CAS  PubMed  Google Scholar 

  12. Lü, F., Hao, L., Guan, D., Qi, Y., Shao, L., & He, P. (2013). Synergetic stress of acids and ammonium on the shift in the methanogenic pathways during thermophilic anaerobic digestion of organics. Water Research, 47(7), 2297–2306.

    Article  CAS  PubMed  Google Scholar 

  13. Karakashev, D., Batstone, D. J., & Angelidaki, I. (2005). Influence of environmental conditions on methanogenic compositions in anaerobic biogas reactors. Applied and Environmental Microbiology, 71(1), 331–338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Koster, I. W., & Lettinga, G. (1984). The influence of ammonium-nitrogen on the specific activity of pelletized methanogenic sludge. Agricutural Wastes, 9(3), 205–216.

    Article  CAS  Google Scholar 

  15. Schink, B. (1997). Energetics of syntrophic cooperation in methanogenic degradation. Microbiology and Molecular Biology Reviews, 61(2), 262–280.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Kida, K., Morimura, S., & Sonoda, Y. (1993). Accumulation of propionic acid during anaerobic treatment of distillery wastewater from barley-Shochu making. Journal of Fermentation and Bioengineering, 75(3), 213–216.

    Article  CAS  Google Scholar 

  17. Li, Y., Zhang, Y., Kong, X., Li, L., Yuan, Z., Dong, R., & Sun, Y. (2017). Effects of ammonia on propionate degradation and microbial community in digesters using propionate as a sole carbon source. Journal of Chemical Technology and Biotechnology, 92(10), 2538–2545.

    Article  CAS  Google Scholar 

  18. Del Giorgio, P. A., & Gasol, J. M. (2008). Physiological structure and single-cell activity in marine bacterioplankton. Microbial Ecology of the Oceans, 2, 243–285.

    Article  Google Scholar 

  19. Bremer, H., & Dennis, P. P. (1996). In Neidhardt et al. (Eds.), In Escherichia coli and Salmonella typhimurium: cellular and molecular biology, chapter. 97: Modulation of Chemical Composition and Other Parameters of the Cell by Growth Rate (pp. 1553–1569).

    Google Scholar 

  20. Shigematsu, T., Tang, Y., Kawaguchi, H., Ninomiya, K., Kijima, J., Kobayashi, T., Morimura, S., & Kida, K. (2003). Effect of dilution rate on structure of a mesophilic acetate-degrading methanogenic community during continuous cultivation. Journal of Bioscience and Bioengineering, 96(6), 547–558.

    Article  CAS  PubMed  Google Scholar 

  21. Griffiths, R. I., Whiteley, A. S., O'Donnell, A. G., & Bailey, M. J. (2000). Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA-and rRNA-based microbial community composition. Applied and Environmental Microbiology, 66(12), 5488–5491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Dan, X., Chen, H., Chen, F., He, Y., Zhao, C., Zhu, D., Zeng, L., & Li, W. (2016). Analysis of the rumen bacteria and methanogenic archaea of yak (Bos grunniens) steers grazing on the Qinghai-Tibetan Plateau. Livestock Science, 188, 61–71.

    Article  Google Scholar 

  23. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16), 2194–2200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261–5267.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Jiang, X., Hayashi, J., Sun, Z. Y., Yang, L., Tang, Y. Q., Oshibe, H., Osaka, N., & Kida, K. (2013). Improving biogas production from protein-rich distillery wastewater by decreasing ammonia inhibition. Process Biochemistry, 48(11), 1778–1784.

    Article  CAS  Google Scholar 

  26. Barberán, A., Bates, S. T., Casamayor, E. O., & Fierer, N. (2011). Using network analysis to explore co-occurrence patterns in soil microbial communities. The ISME Journal, 6, 343.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Campanaro, S., Treu, L., Kougias, P. G., Luo, G., & Angelidaki, I. (2018). Metagenomic binning reveals the functional roles of core abundant microorganisms in twelve full-scale biogas plants. Water Research, 140, 123–134.

    Article  CAS  PubMed  Google Scholar 

  28. Alsouleman, K., Linke, B., Klang, J., Klocke, M., Krakat, N., & Theuerl, S. (2016). Reorganisation of a mesophilic biogas microbiome as response to a stepwise increase of ammonium nitrogen induced by poultry manure supply. Bioresource Technology, 208, 200–204.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  30. Parkin, G. F., Lynch, N. A., Kuo, W.-C., Van Keuren, E. L., & Bhattacharya, S. K. (1990). Interaction between sulfate reducers and methanogens fed acetate and propionate. Research Journal of the Water Pollution Control Federation, 62, 780–788.

    CAS  Google Scholar 

  31. Poirier, S., Desmond-Le Quéméner, E., Madigou, C., Bouchez, T., & Chapleur, O. (2016). Anaerobic digestion of biowaste under extreme ammonia concentration: Identification of key microbial phylotypes. Bioresource Technology, 207, 92–101.

    Article  CAS  PubMed  Google Scholar 

  32. Procházka, J., Dolejš, P., Máca, J., & Dohányos, M. (2012). Stability and inhibition of anaerobic processes caused by insufficiency or excess of ammonia nitrogen. Applied Microbiology and Biotechnology, 93(1), 439–447.

    Article  CAS  PubMed  Google Scholar 

  33. de Bok, F. A. M., Stams, A. J. M., Dijkema, C., & Boone, D. R. (2001). Pathway of propionate oxidation by a syntrophic culture of Smithella propionica and Methanospirillum hungatei. Applied and Environmental Microbiology, 67(4), 1800–1804.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Houwen, F. P., Plokker, J., Stams, A. J. M., & Zehnder, A. J. B. (1990). Enzymatic evidence for involvement of the methylmalonyl-CoA pathway in propionate oxidation by Syntrophobacter wolinii. Archives of Microbiology, 155(1), 52–55.

    Article  CAS  Google Scholar 

  35. Plugge, C. M., Dijkema, C., & Stams, A. J. M. (1993). Acetyl-CoA cleavage pathway in a syntrophic propionate oxidizing bacterium growing on fumarate in the absence of methanogens. FEMS Microbiology Letters, 110(1), 71–76.

    Article  CAS  Google Scholar 

  36. Nobu, M. K., Narihiro, T., Rinke, C., Kamagata, Y., Tringe, S. G., Woyke, T., & Liu, W. (2015). Microbial dark matter ecogenomics reveals complex synergistic network in a methanogenic bioreactor. The ISME Journal, 9(8), 1710–1722.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Beckmann, S., Lueders, T., Krüger, M., von Netzer, F., Engelen, B., & Cypionka, H. (2011). Acetogens and acetoclastic Methanosarcinales govern methane formation in abandoned coal mines. Applied and Environmental Microbiology, 77(11), 3749–3756.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kimura, Z.-i., & Okabe, S. (2013). Acetate oxidation by syntrophic association between Geobacter sulfurreducens and a hydrogen-utilizing exoelectrogen. The ISME Journal, 7(8), 1472–1482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Calli, B., Mertoglu, B., Inanc, B., & Yenigun, O. (2005). Effects of high free ammonia concentrations on the performances of anaerobic bioreactors. Process Biochemistry, 40(3–4), 1285–1292.

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the Ministry of Science and Technology of China (2016YFE0127700) and the National Natural Science Foundation of China (51678378). This study was partly supported by the Japan Society for the Promotion of Science with Grant-in-Aid for Scientific Research No. 17H05239, 18H01576 and 18H03367.

Author information

Authors and Affiliations

  1. College of Architecture and Environment, Sichuan University, No. 24, South Section 1, First Ring Road, Chengdu, 610065, Sichuan, China

    Hui-Zhong Wang, Min Gou, Yue Yi, Zi-Yuan **a & Yue-Qin Tang

  2. Institute of New Energy and Low-Carbon Technology, Sichuan University, No. 24, South Section 1, First Ring Road, Chengdu, 610065, Sichuan, China

    Ying-Chun Yan & Yue-Qin Tang

  3. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan

    Masaru K Nobu & Takashi Narihiro

Authors
  1. Hui-Zhong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying-Chun Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Gou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yue Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zi-Yuan **a
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Masaru K Nobu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Takashi Narihiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yue-Qin Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yue-Qin Tang.

Ethics declarations

Human and Animal Rights and Informed Consent

This paper does not contain any studies with human participants or animals performed by any of the authors.

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOC 1614 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, HZ., Yan, YC., Gou, M. et al. Response of Propionate-Degrading Methanogenic Microbial Communities to Inhibitory Conditions. Appl Biochem Biotechnol 189, 233–248 (2019). https://doi.org/10.1007/s12010-019-03005-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-019-03005-1

Keywords

Search

Navigation