How resistant is anammox biofilm against antibiotics: A special insight into anammox response towards fluoroquinolones

Faysal-Al Mamun; Rohit Kumar; Kelvin Ugochukwu Anwuta; Sovik Das; Madis Jaagura; Koit Herodes; Tetyana Kyrpel; Agnieszka Fiszka Borzyszkowska; Anna Zielińska-Jurek; Zane Vincevica-Gaile; Juris Burlakovs; Andrey E Krauklis; Mohamad Nor Azra; Md Salauddin; Jiexi Zhong; Taavo Tenno; Kai Bester; Ivar Zekker

doi:10.1016/j.heliyon.2024.e41339

How resistant is anammox biofilm against antibiotics: A special insight into anammox response towards fluoroquinolones

Heliyon. 2024 Dec 18;11(1):e41339. doi: 10.1016/j.heliyon.2024.e41339. eCollection 2025 Jan 15.

Authors

Faysal-Al Mamun¹, Rohit Kumar¹, Kelvin Ugochukwu Anwuta¹, Sovik Das², Madis Jaagura³, Koit Herodes⁴, Tetyana Kyrpel⁴, Agnieszka Fiszka Borzyszkowska⁵, Anna Zielińska-Jurek⁶, Zane Vincevica-Gaile⁷, Juris Burlakovs⁸, Andrey E Krauklis⁹, Mohamad Nor Azra¹⁰, Md Salauddin¹¹, Jiexi Zhong¹², Taavo Tenno¹, Kai Bester^{12

13}, Ivar Zekker¹

Affiliations

¹ Institute of Chemistry, University of Tartu, 14a Ravila St., 50411, Tartu, Estonia.
² Indian Institute of Technology Delhi, Hauz Khas, New Delhi, 110 016, India.
³ Institute of Genomics, University of Tartu, Riia 23b, Tartu, 51010, Estonia.
⁴ Institute of Chemistry, Chair of Analytics, University of Tartu, 14a Ravila St., 50411, Tartu, Estonia.
⁵ Department of Environmental Toxicology, Faculty of Health Sciences, Medical University of Gdansk, Dębowa Str. 23A, 80-204, Gdansk, Poland.
⁶ Department of Process Engineering and Chemical Technology, Gdansk University of Technology, Narutowicza 11/12, 80-233, Gdansk, Poland.
⁷ Department of Environmental Science, University of Latvia, Jelgavas Street 1, LV-1004, Riga, Latvia.
⁸ Faculty of Civil and Mechanical Engineering, Riga Technical University, LV-1048, Riga, Latvia.
⁹ ASEMlab - Laboratory of Advanced and Sustainable Engineering Materials, Department of Manufacturing and Civil Engineering, NTNU - Norwegian University of Science and Technology, 2815, Gjøvik, Norway.
¹⁰ Institute of Climate Adaptation and Marine Biotechnology, Universiti Malaysia Terengganu, 21030, Kuala Nerus, Terengganu, Malaysia.
¹¹ UCD Dooge Centre for Water Resources Research, School of Civil Engineering, University College Dublin, Ireland.
¹² Department of Environmental Science, Aarhus University, Frederiksborgvej 399, Roskilde, 4000, Denmark.
¹³ WATEC - Centre for Water Technology, Aarhus University, Ny Munkegade 120, Aarhus, 8000, Denmark.

Abstract

Elevated concentrations of pharmaceutically active compounds (PhACs) in the water bodies are posing a serious threat to the aquatic microbiota and other organisms. In this context, anaerobic ammonium oxidizing (anammox) bacteria carry a great potential to degrade PhACs through their innate metabolic pathways. This study investigates the influence of short-term exposure to lower and higher concentrations (0.8 mg L^-1, 0.06 mg L^-1, respectively) of antibiotics on the anammox process under distinct operational conditions (starvation/non-starvation) in moving bed biofilm reactor (MBBR). During batch operations that lasted for up to 6 h, the total nitrogen removal efficiency (TNRE) and total nitrogen conversion rate (TNCR) reached a maximum of 93 ± 5 % and 6.97 ± 1.30 mg N g^-1 TSS d^-1, respectively. Evidently, at higher PhAC levels, the anammox process was active, and up to 75 % PhAC removal efficiency was obtained within 6 h of the batch cycle. Most importantly, the anammox biofilm effectively eliminated the PhACs compounds, i.e., ciprofloxacin (CIP), ofloxacin (OFL), and norfloxacin (NOR) present at higher (0.8 mg L^-1) and lower (0.06 mg L^-1) total PhACs (sum of CIP, NOR, OFL) concentrations. Furthermore, 16S rRNA sequencing analyses showed a mixture of nitrifying, denitrifying, and anammox bacterial commodities enriched on the carriers' surface with a high relative abundance of Candidatus Brocadia, primarily responsible for catalyzing the anammox process. This study showed the intricate relationship between PhAC concentrations, TNCR, and antibiotic elimination in the wastewater treatment, and the results obtained set up a new breakthrough in wastewater treatment. Future research should investigate the mechanisms that underlie the anammox biofilms' resistance to various types of PhACs and investigate the long-term stability and scalability of this process with real wastewater influents.

Keywords: Adsorption; Anammox; Moving bed biofilm reactor; Nitrogen removal; Pharmaceutically active compounds.