Synergistic mechanism of tetracycline degradation by poor-degrading microbe Serratia marcescens cooperated with insect during environmental decomposition cycle

Chongrui Yang; Zhengzheng Zhao; Chen Sun; Bingqi Gao; Yushi Wu; Mengzhe Li; Liu Chen; Yan Ju; Kashif Ur Rehman; Chan Yu; Qinfen Li; Arnold van Huis; Núria Jimenez; Longyu Zheng; Feng Huang; Zhuqing Ren; Ziniu Yu; Yongping Huang; Jibin Zhang; Minmin Cai

doi:10.1016/j.biortech.2025.132887

Synergistic mechanism of tetracycline degradation by poor-degrading microbe Serratia marcescens cooperated with insect during environmental decomposition cycle

Bioresour Technol. 2025 Jun 25:132887. doi: 10.1016/j.biortech.2025.132887. Online ahead of print.

Authors

Chongrui Yang¹, Zhengzheng Zhao¹, Chen Sun¹, Bingqi Gao¹, Yushi Wu¹, Mengzhe Li¹, Liu Chen¹, Yan Ju¹, Kashif Ur Rehman², Chan Yu³, Qinfen Li⁴, Arnold van Huis⁵, Núria Jimenez⁶, Longyu Zheng¹, Feng Huang¹, Zhuqing Ren⁷, Ziniu Yu¹, Yongping Huang⁸, Jibin Zhang⁹, Minmin Cai¹⁰

Affiliations

¹ National Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, National Engineering Research Center of Microbial Pesticides, Huazhong Agricultural University, Wuhan 430070, PR China; Frontiers Science Center for Animal Breeding and Sustainable Production, Wuhan 430070, PR China; Hubei Hongshan Laboratory, Wuhan 430070, PR China.
² German Institute of Food Technologies (DIL e.V.), Prof.-v.-Klitzing-Str. 7, 49610 Quakenbrück, Germany; Department of Microbiology, Faculty of Veterinary and Animal Sciences, The Islamia University of Bahawalpur, Bahawalpur 63100, Pakistan.
³ State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan 430062, PR China.
⁴ Environmental and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, PR China.
⁵ Laboratory of Entomology, Wageningen University & Research, Droevendaalsesteeg, Wageningen 6708 PB, Netherlands.
⁶ Department of Chemical Engineering, Vilanova i la Geltrú School of Engineering (EPSEVG), Universitat Polit ecnica de Catalunya⋅BarcelonaTech, Vilanova i la Geltrú, 08800, Spain.
⁷ Frontiers Science Center for Animal Breeding and Sustainable Production, Wuhan 430070, PR China; Hubei Hongshan Laboratory, Wuhan 430070, PR China.
⁸ School of Environmental Science and Engineering, Shanghai Jiao Tong University, Shanghai 200000, PR China. Electronic address: insectgroup@sjtu.edu.cn.
⁹ National Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, National Engineering Research Center of Microbial Pesticides, Huazhong Agricultural University, Wuhan 430070, PR China; Frontiers Science Center for Animal Breeding and Sustainable Production, Wuhan 430070, PR China; Hubei Hongshan Laboratory, Wuhan 430070, PR China. Electronic address: zhangjb@mail.hzau.edu.cn.
¹⁰ National Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, National Engineering Research Center of Microbial Pesticides, Huazhong Agricultural University, Wuhan 430070, PR China; Frontiers Science Center for Animal Breeding and Sustainable Production, Wuhan 430070, PR China; Hubei Hongshan Laboratory, Wuhan 430070, PR China. Electronic address: cmm114@mail.hzau.edu.cn.

PMID: 40578705
DOI: 10.1016/j.biortech.2025.132887

Abstract

The antibiotic residues in the environment disrupts ecological stability, ultimately poses potential risks to human health through the spread of the food chain. The degradation of antibiotics by insects is a crucial part of the environmental decomposition cycle, especially the synergistic effect between gut microbiota and host, which is a crucial biological principle for insects to alleviate environmental pollutants. It was known that the strain Serratia marcescens BSFL-6 efficiently degrade tetracycline collaborated with its host black soldier fly larvae, but the potential biological mechanism is still unclear. S. marcescens BSFL-6 mono-associated larvae (BML) tetracycline degradation system was performed for investigating the synergistic mechanism. Multiple key functional genes responsible for tetracycline synergistic degradation were analyzed through genome and transcriptome. Through overexpression and RNAi, results revealed that tet34 and UGT2B7 in S. marcescens BSFL-6 and larvae are the principal genes involved in tetracycline synergistic metabolism. Xanthine phosphoribosyltransferase (SmXPRTase) and UDP glucuronosyltransferase (HiUGTase) encoded by tet34 and UGT2B7 respectively exhibit the tetracycline metabolism function which scarcely reported. Through comprehensive analysis of tetracycline metabolites and in vitro purification of key enzymes, it could be reasonably inferred that SmXPRTase firstly participates in the degradation of tetracycline by removing dimethylamino to produce P430. Subsequently, HiUGTase metabolises P430 into bioavailable P652 through the glucuronidation, playing a crucial role in the overall degrading process. An undisclosed mechanism in degrading tetracycline by gut microbe collaborated with host was revealed, which contributes a new insight for the remediation mechanism of antibiotic contamination in the environment by insects.

Keywords: Black soldier fly larvae; Functional genes; Intestinal microbes; Synergistic degradation of tetracycline.