Advanced searchCitation search
Skip main navigation
Close Drawer MenuOpen Drawer Menu
Previous article
Next article
Technical Papers
Feb 26, 2024

Exploring the Influence of Sulfide on Nitrogen-Removal Performance in Anammox Processes: An Investigation of Short-Term and Long-Term Effects

Authors: Magray Owaes [email protected], Khalid Muzamil Gani, A.M.ASCE https://orcid.org/0000-0002-2062-1547 [email protected], Sheena Kumari [email protected], Mohammed Seyam [email protected], and Faizal Bux [email protected]Author Affiliations
Publication: Journal of Environmental Engineering
Volume 150, Issue 5
https://doi.org/10.1061/JOEEDU.EEENG-7570
Get Access

Abstract

Sulfide-based pathways for generating nitrite to sustain anaerobic ammonium oxidation (anammox) have garnered increasing attention. However, the presence of sulfide can also impact the anammox process, necessitating a comprehensive understanding of both its short-term and long-term effects on anammox. This study aimed to investigate the influence of sulfide on anammox, including its effects on the microbial community and process kinetics. During long-term operation, the maximum sulfide dosage tested was 30  mg S/L over 50 days of operation, exhibiting good nitrogen removal efficiency of 83.9%±4.8%. Conversely, under short-term exposure to sulfide, nitrogen removal efficiency was notably affected, decreasing to 68.98% at a considerably lower sulfide concentration of only 16  mg S/L. Within the context of long-term sulfide exposure, the maximum contribution of anammox to nitrogen removal reached 86.72% at a sulfide dosage of 25  mg S/L. However, when the influent sulfide concentration was increased to 50  mg/L, the contribution of anammox to nitrogen removal sharply declined to 41.3%. Microbial community analysis revealed as the sulfide concentration increased from 8 to 16  mg S/L, the abundance of anammox bacteria decreased from 2.46×105 to 1.67×105 copies/mL, whereas the abundance of Nitrobacter spp. increased from 2.73×102 to 8.13×102 copies/mL. However, during long-term operation, there was a more pronounced decrease in the microbial abundance of anammox, reducing from 5.3×105 to 3.77×102  copies/mL. Taking this decrease together with the improved efficiency of anammox observed during long-term operation, these findings suggest that sulfide’s influence on anammox primarily impacts its metabolic activity rather than its microbial abundance.

Get full access to this article

View all available purchase options and get full access to this article.

Get Access

Data Availability Statement

Data are available from the corresponding author upon reasonable request.

Acknowledgments

We acknowledge the financial support from the South African Research Chair Initiative (SARChI) of the Department of Science and Technology, and the National Research Foundation of South Africa (Grant No. 84166). This study was also funded by Water Research Commission, South Africa (C2019/2020-00103).
Author contributions: Magray Owaes: Conceptualization, Data analysis, Writing–original draft. Khalid Muzamil Gani: Data analysis, Supervision, Finalized manuscript contents, Edited the manuscript. Sheena Kumari: Supervision, Writing–reviewing and editing. Mohammed Seyam: Supervision, Validation. Faizal Bux: Supervision, Validation.

References

APHA (American Public Health Association). 2005. Standard methods for the examination of water and wastewater. Washington, DC: APHA.
Google Scholar
Avrahami, S., Z. Jia, J. D. Neufeld, J. C. Murrell, R. Conrad, and K. Küsel. 2011. “Active autotrophic ammonia-oxidizing bacteria in biofilm enrichments from simulated creek ecosystems at two ammonium concentrations respond to temperature manipulation.” Appl. Environ. Microbiol. 77 (20): 7329–7338. https://doi.org/10.1128/AEM.05864-11.
Google Scholar
Carvajal-Arroyo, J. M., W. Sun, R. Sierra-Alvarez, and J. A. Field. 2013. “Inhibition of anaerobic ammonium oxidizing (anammox) enrichment cultures by substrates, metabolites and common wastewater constituents.” Chemosphere 91 (1): 22–27. https://doi.org/10.1016/j.chemosphere.2012.11.025.
Google Scholar
Chen, H., Z. Tu, S. Wu, G. Yu, C. Du, H. Wang, E. Yang, L. Zhou, B. Deng, and D. Wang. 2021. “Recent advances in partial denitrification-anaerobic ammonium oxidation process for mainstream municipal wastewater treatment.” Chemosphere 278 (Apr): 130436. https://doi.org/10.1016/j.chemosphere.2021.130436.
Google Scholar
Dapena-Mora, A., I. Fernandez, J. L. Campos, A. Mosquera-Corral, R. Mendez, and M. S. M. Jetten. 2007. “Evaluation of activity and inhibition effects on Anammox process by batch tests based on the nitrogen gas production.” Enzyme Microb. Technol. 40 (4): 859–865. https://doi.org/10.1016/j.enzmictec.2006.06.018.
Google Scholar
Deng, Y. F., F. X. Zan, H. Huang, D. Wu, W. T. Tang, and G. H. Chen. 2022. “Coupling sulfur-based denitrification with anammox for effective and stable nitrogen removal: A review.” Water Res. 224: 119051. https://doi.org/10.1016/j.watres.2022.119051.
Google Scholar
Dionisi, H. M., A. C. Layton, G. Harms, I. R. Gregory, K. G. Robinson, and G. S. Sayler. 2002. “Quantification of Nitrosomonas oligotropha-like ammonia-oxidizing bacteria and Nitrospira spp. from full-scale wastewater treatment plants by competitive PCR.” Appl. Environ. Microbiol. 68 (1): 245–253. https://doi.org/10.1128/AEM.68.1.245-253.2002.
Google Scholar
Jensen, M. M., P. Lam, N. P. Revsbech, B. Nagel, B. Gaye, M. S. Jetten, and M. M. Kuypers. 2011. “Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium.” ISME J. 5 (10): 1660–1670. https://doi.org/10.1038/ismej.2011.44.
Google Scholar
Jin, R. C., G. F. Yang, J. J. Yu, and P. Zheng. 2012. “The inhibition of the Anammox process: A review.” Chem. Eng. J. 197 (Apr): 67–79. https://doi.org/10.1016/j.cej.2012.05.014.
Google Scholar
Jin, R. C., G. F. Yang, Q. Q. Zhang, C. Ma, J. J. Yu, and B. S. Xing. 2013a. “The effect of sulfide inhibition on the ANAMMOX process.” Water Res. 47 (3): 1459–1469. https://doi.org/10.1016/j.watres.2012.12.018.
Google Scholar
Jin, R. C., Q. Q. Zhang, G. F. Yang, B. S. Xing, Y. X. Ji, and H. Chen. 2013b. “Evaluating the recovery performance of the ANAMMOX process following inhibition by phenol and sulfide.” Bioresour. Technol. 142 (Sep): 162–170. https://doi.org/10.1016/j.biortech.2013.05.022.
Google Scholar
Jin, T., T. Zhang, L. Ye, O. O. Lee, Y. H. Wong, and P. Y. Qian. 2011. “Diversity and quantity of ammonia-oxidizing Archaea and Bacteria in sediment of the Pearl River Estuary, China.” Appl. Microbiol. Biotechnol. 90: 1137–1145.
Crossref
Google Scholar
Kalyuzhnyi, S., M. Gladchenko, A. Mulder, and B. Versprille. 2006. “DEAMOX—New biological nitrogen removal process based on anaerobic ammonia oxidation coupled to sulphide-driven conversion of nitrate into nitrite.” Water Res. 40 (19): 3637–3645. https://doi.org/10.1016/j.watres.2006.06.010.
Google Scholar
Kartal, B., and J. T. Keltjens. 2016. “Anammox biochemistry: A tale of heme c proteins.” Trends Biochem. Sci. 41 (12): 998–1011. https://doi.org/10.1016/j.tibs.2016.08.015.
Google Scholar
Klotz, M. G., and L. Y. Stein. 2008. “Nitrifier genomics and evolution of the nitrogen cycle.” FEMS Microbiol. Lett. 278 (2): 146–156. https://doi.org/10.1111/j.1574-6968.2007.00970.x.
Google Scholar
Lackner, S., E. M. Gilbert, S. E. Vlaeminck, A. Joss, H. Horn, and M. C. M. van Loosdrecht. 2014. “Full-scale partial nitritation/anammox experiences–An application survey.” Water Res. 55 (Apr): 292–303. https://doi.org/10.1016/j.watres.2014.02.032.
Google Scholar
Lazarova, V., C. Peregrina, and D. Pascal. 2012. “Towards energy selfsufficiency of wastewater treatment.” In Water. Energy interactions in water reuse, 87–126. London: IWA Publishing.
Google Scholar
Liang, Z., J. Shi, W. Yang, L. Dai, and X. Dai. 2022. “Coupling anammox and feammox via polymeric ferric sulfate: An efficient and aeration-saving way for nitrogen removal.” J. Cleaner Prod. 355 (Aug): 131788. https://doi.org/10.1016/j.jclepro.2022.131788.
Google Scholar
Liu, C., D. Zhao, L. Yan, A. Wang, Y. Gu, and D. J. Lee. 2015. “Elemental sulfur formation and nitrogen removal from wastewaters by autotrophic denitrifiers and anammox bacteria.” Bioresour. Technol. 191 (Jun): 332–336. https://doi.org/10.1016/j.biortech.2015.05.027.
Google Scholar
Lotti, T., R. Kleerebezem, J. M. Abelleira-Pereira, B. Abbas, and M. C. M. Van Loosdrecht. 2015. “Faster through training: The anammox case.” Water Res. 81 (Dec): 261–268. https://doi.org/10.1016/j.watres.2015.06.001.
Google Scholar
Miao, Y., L. Zhang, B. Li, Q. Zhang, S. Wang, and Y. Peng. 2017. “Enhancing ammonium oxidizing bacteria activity was key to single-stage partial nitrification-anammox system treating low-strength sewage under intermittent aeration condition.” Bioresour. Technol. 231 (Apr): 36–44. https://doi.org/10.1016/j.biortech.2017.01.045.
Google Scholar
Mulder, A., A. A. Van de Graaf, L. A. Robertson, and J. G. Kuenen. 1995. “Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor.” FEMS Microbiol. Ecol. 16 (3): 177–184. https://doi.org/10.1111/j.1574-6941.1995.tb00281.x.
Google Scholar
Park, B. J., S. J. Park, D. N. Yoon, S. Schouten, J. S. Sinninghe Damsté, and S. K. Rhee. 2010. “Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria.” Appl. Environ. Microbiol. 76 (22): 7575–7587. https://doi.org/10.1128/AEM.01478-10.
Google Scholar
Pietri, R., E. Román-Morales, and J. López-Garriga. 2011. “Hydrogen sulfide and hemeproteins: Knowledge and mysteries.” Antioxid. Redox Signaling 15 (2): 393–404. https://doi.org/10.1089/ars.2010.3698.
Google Scholar
Rodríguez-Gómez, L. E., J. Rodríguez-Sevilla, A. Hernández, and M. Álvarez. 2021. “Factors affecting nitrification with nitrite accumulation in treated wastewater by oxygen injection.” Environ. Technol. 42 (5): 813–825. https://doi.org/10.1080/09593330.2019.1645742.
Google Scholar
Rothrock, M. J., M. B. Vanotti, A. A. Szögi, M. C. G. Gonzalez, and T. Fujii. 2011. “Long-term preservation of anammox bacteria.” Appl. Microbiol. Biotechnol. 92 (1): 147–157. https://doi.org/10.1007/s00253-011-3316-1.
Google Scholar
Russ, L., D. R. Speth, M. S. M. Jetten, H. J. M. Op den Camp, and B. Kartal. 2014. “Interactions between anaerobic ammonium and sulfur-oxidizing bacteria in a laboratory scale model system.” Environ. Microbiol. 16 (11): 3487–3498. https://doi.org/10.1111/1462-2920.12487.
Google Scholar
Schmid, M. C., A. B. Hooper, M. G. Klotz, D. Woebken, P. Lam, M. M. Kuypers, A. Pommerening-Roeser, H. J. Op Den Camp, and M. S. Jetten. 2008. “Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria.” Environ. Microbiol. 10 (11): 3140–3149. https://doi.org/10.1111/j.1462-2920.2008.01732.x.
Google Scholar
Strous, M., J. G. Kuenen, J. A. Fuerst, M. Wagner, and M. S. Jetten. 2002. “The anammox case—A new experimental manifesto for microbiological eco-physiology.” Antonie van Leeuwenhoek 81 (1–4): 693–702. https://doi.org/10.1023/A:1020590413079.
Google Scholar
Tong, T., J. Tong, K. Xue, Y. Li, J. Yu, and Y. Wei. 2023. “Microbial community structure and functional prediction in five full-scale industrial park wastewater treatment plants.” Sci. Total Environ. 904 (Dec): 166529. https://doi.org/10.1016/j.scitotenv.2023.166529.
Google Scholar
Van de Graaf, A. A., P. de Bruijn, L. A. Robertson, M. S. Jetten, and J. G. Kuenen. 1996. “Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor.” Microbiology 142 (8): 2187–2196. https://doi.org/10.1099/13500872-142-8-2187.
Google Scholar
Van der Star, W. R., W. R. Abma, D. Blommers, J. W. Mulder, T. Tokutomi, M. Strous, C. Picioreanu, and M. C. van Loosdrecht. 2007. “Startup of reactors for anoxic ammonium oxidation: Experiences from the first full-scale anammox reactor in Rotterdam.” Water Res. 41 (18): 4149–4163. https://doi.org/10.1016/j.watres.2007.03.044.
Google Scholar
Wang, H., C. Chen, E. Yang, Z. Tu, J. Liang, X. Dai, and H. Chen. 2022. “Revealing the effect of biofilm formation in partial nitritation-anammox systems: Start-up, performance stability, and recovery.” Bioresour. Technol. 357 (Apr): 127379. https://doi.org/10.1016/j.biortech.2022.127379.
Google Scholar
Wisniewski, K., A. Di Biase, G. Munz, J. A. Oleszkiewicz, and J. Makinia. 2019. “Kinetic characterization of hydrogen sulfide inhibition of suspended anammox biomass from a membrane bioreactor.” Biochem. Eng. J. 143 (Feb): 48–57. https://doi.org/10.1016/j.bej.2018.12.015.
Google Scholar
Yang, G. F., and R. C. Jin. 2013. “Reactivation of effluent granular sludge from a high-rate Anammox reactor after storage.” Biodegradation 24 (1): 13–32. https://doi.org/10.1007/s10532-012-9554-9.
Google Scholar
Yang, S., Y. Peng, S. Zhang, X. Han, J. Li, and L. Zhang. 2021. “Carrier type induces anammox biofilm structure and the nitrogen removal pathway: Demonstration in a full-scale partial nitritation/anammox process.” Bioresour. Technol. 334 (Jun): 125249. https://doi.org/10.1016/j.biortech.2021.125249.
Google Scholar
Yuan, Y., X. Li, and B. L. Li. 2020. “Autotrophic nitrogen removal characteristics of PN-anammox process enhanced by sulfur autotrophic denitrification under mainstream conditions.” Bioresour. Technol. 316 (Nov): 123926. https://doi.org/10.1016/j.biortech.2020.123926.
Google Scholar
Zhang, Q., J. J. Fu, J. T. Zhang, Y. H. Zhao, L. Y. Jin, N. S. Fan, B. C. Huang, and R. C. Jin. 2020. “Deciphering the microbial community and functional genes response of anammox sludge to sulfide stress.” Bioresour. Technol. 302 (Jun): 122885. https://doi.org/10.1016/j.biortech.2020.122885.
Google Scholar
Zhang, Y., S. Ji, P. Xie, Y. Liang, H. Chen, L. Chen, C. Wei, Z. Yang, and G. Qiu. 2023. “Simultaneous partial nitrification, Anammox and nitrate-dependent Fe(II) oxidation (NDFO) for total nitrogen removal under limited dissolved oxygen and completely autotrophic conditions.” Sci. Total Environ. 880 (Apr): 163300. https://doi.org/10.1016/j.scitotenv.2023.163300.
Google Scholar

Information & Authors

Information

Published In

Go to Journal of Environmental Engineering
Journal of Environmental Engineering
Volume 150 • Issue 5 • May 2024

Copyright

© 2024 American Society of Civil Engineers.

History

Received: Sep 21, 2023
Accepted: Dec 1, 2023
Published online: Feb 26, 2024
Published in print: May 1, 2024
Discussion open until: Jul 26, 2024

Permissions

Request permissions for this article.

ASCE Technical Topics:

  1. [Inorganic compounds]
  2. Ammonia
  3. Anaerobic processes
  4. Biological processes
  5. Chemical compounds
  6. Chemical elements
  7. Chemical processes
  8. Chemicals
  9. Chemistry
  10. Continuum mechanics
  11. Dynamics (solid mechanics)
  12. Engineering mechanics
  13. Environmental engineering
  14. Kinetics
  15. Microbes
  16. Nitrogen
  17. Nutrient pollution
  18. Organic compounds
  19. Organisms
  20. Oxidation
  21. Pollution
  22. Salts
  23. Solid mechanics
  24. Sulfides
  25. Waste management
  26. Water pollution

Authors

Affiliations

Magray Owaes [email protected]
Postdoc, Institute for Water and Wastewater Technology, Durban Univ. of Technology, PO Box 1334, Durban 4000, South Africa. Email: [email protected]
View all articles by this author
Khalid Muzamil Gani, A.M.ASCE https://orcid.org/0000-0002-2062-1547 [email protected]
Assistant Professor, Dept. of Civil Engineering, National Institute of Technology, Srinagar, Jammu and Kashmir 190006, India; Honorary Research Associate, Institute for Water and Wastewater Technology, Durban Univ. of Technology, PO Box 1334, Durban 4000, South Africa. ORCID: https://orcid.org/0000-0002-2062-1547. Email: [email protected]
View all articles by this author
Sheena Kumari [email protected]
Professor, Institute for Water and Wastewater Technology, Durban Univ. of Technology, PO Box 1334, Durban 4000, South Africa. Email: [email protected]
View all articles by this author
Mohammed Seyam [email protected]
Senior Lecturer, Dept. of Civil Engineering and Geomatics, Durban Univ. of Technology, PO Box 1334, Durban 4000, South Africa. Email: [email protected]
View all articles by this author
Faizal Bux [email protected]
Professor, Institute for Water and Wastewater Technology, Durban Univ. of Technology, PO Box 1334, Durban 4000, South Africa (corresponding author). Email: [email protected]
View all articles by this author

Metrics & Citations

Metrics

Citations

Download citation

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

View Options

Get Access

Access content

Please select your options to get access

Log in/Register Log in via your institution (Shibboleth)
ASCE Members: Please log in to see member pricing

Purchase

Save for later Information on ASCE Library Cards
ASCE Library Cards let you download journal articles, proceedings papers, and available book chapters across the entire ASCE Library platform. ASCE Library Cards remain active for 24 months or until all downloads are used. Note: This content will be debited as one download at time of checkout.

Terms of Use: ASCE Library Cards are for individual, personal use only. Reselling, republishing, or forwarding the materials to libraries or reading rooms is prohibited.
ASCE Library Card (5 downloads)
$105.00
Add to cart
ASCE Library Card (20 downloads)
$280.00
Add to cart
Buy Single Article
$35.00
Add to cart

Get Access

Access content

Please select your options to get access

Log in/Register Log in via your institution (Shibboleth)
ASCE Members: Please log in to see member pricing

Purchase

Save for later Information on ASCE Library Cards
ASCE Library Cards let you download journal articles, proceedings papers, and available book chapters across the entire ASCE Library platform. ASCE Library Cards remain active for 24 months or until all downloads are used. Note: This content will be debited as one download at time of checkout.

Terms of Use: ASCE Library Cards are for individual, personal use only. Reselling, republishing, or forwarding the materials to libraries or reading rooms is prohibited.
ASCE Library Card (5 downloads)
$105.00
Add to cart
ASCE Library Card (20 downloads)
$280.00
Add to cart
Buy Single Article
$35.00
Add to cart

Media

Figures

Other

Tables

Share

Share

Copy the content Link

Share with email

Email a colleague

Share