Antibiotic resistance genes in food wastes: diversity, dynamics, and interactions with prokaryotes and viruses in centralized biogas plants

Chao Zhang , Jiawei Sun , Zhijian Shi , Meichen Sun , Qianqi Shao , Shicheng Zhang , Gang Luo

ENG. Environ. ›› 2026, Vol. 20 ›› Issue (8) : 117

PDF (4066KB)
ENG. Environ. ›› 2026, Vol. 20 ›› Issue (8) :117 DOI: 10.1007/s11783-026-2217-6
RESEARCH ARTICLE
Antibiotic resistance genes in food wastes: diversity, dynamics, and interactions with prokaryotes and viruses in centralized biogas plants
Author information +
History +
PDF (4066KB)

Abstract

Anaerobic digestion (AD) is widely considered an effective approach for the treatment of food waste (FW). However, the diversity of antibiotic resistance genes (ARGs) in FW, together with ARG dynamics and their interactions with prokaryotes and DNA viruses during AD, remain insufficiently explored. This study performed metagenomic analyses of FW and digestate samples collected from 9 centralized biogas plants. The results showed that FW served as an important reservoir of ARGs. Although the distribution patterns of ARGs in FW and digestate differed, MLS, multidrug, tetracycline, aminoglycoside, and bacitracin were the five most abundant ARG types in both FW and digestate. While AD reduced the overall quantity of ARGs, its capacity to markedly decrease ARG abundance was limited. Procrustes analysis revealed associations between ARGs and prokaryotes and DNA viruses. Among the reconstructed prokaryotic metagenome-assembled genomes (180), 130 were identified as carrying ARGs. DNA viruses showed close associations with antibiotic-resistant bacteria (ARB), with viral-host relationships detected between 181 DNA viruses and 77 ARBs. Most of these viruses were temperate DNA viruses, which may indirectly influence ARG distribution by regulating ARB populations. Nevertheless, the contribution of DNA viruses to ARG dissemination appeared limited, given the small number of detected ARG-carrying viruses and the lack of high-risk ARGs.

Graphical abstract

Keywords

Anaerobic digestion / Food waste / Antibiotic resistance genes / DNA viruses / Prokaryotes

Highlight

● FW and digestate are rich in ARGs, with widely shared ARGs present in both.

● AD exerted a more pronounced reduction on ARG diversity than on ARG abundance.

● ARGs distribution was related to both prokaryotic and DNA virus communities.

● A large proportion of ARBs contained DNA viruses, primarily temperate viruses.

● Only a small proportion of ARGs (less than 3%) was carried by DNA viruses.

Cite this article

Download citation ▾
Chao Zhang, Jiawei Sun, Zhijian Shi, Meichen Sun, Qianqi Shao, Shicheng Zhang, Gang Luo. Antibiotic resistance genes in food wastes: diversity, dynamics, and interactions with prokaryotes and viruses in centralized biogas plants. ENG. Environ., 2026, 20(8): 117 DOI:10.1007/s11783-026-2217-6

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ahlgren N A , Ren J , Lu Y Y , Fuhrman J A , Sun F Z . (2017). Alignment-free d2* oligonucleotide frequency dissimilarity measure improves prediction of hosts from metagenomically-derived viral sequences. Nucleic Acids Research, 45(1): 39–53

[2]

Aiyegoro O A , Moyane J N , Adegoke A A , Jideani A I O , Reddy P , Okoh A I . (2023). Virulence signatures, integrons, and antibiotic resistance genes in bacterial strains recovered from selected commercial dairy products and fresh raw meat. Current Microbiology, 80(8): 254

[3]

Arango-Argoty G , Garner E , Pruden A , Heath L S , Vikesland P , Zhang L Q . (2018). DeepARG: a deep learning approach for predicting antibiotic resistance genes from metagenomic data. Microbiome, 6(1): 23

[4]

Bastian MHeymann SJacomy M (2009). Gephi: an open source software for exploring and manipulating networks. In: Proceedings of the 3rd International Conference on Web and Social Media. San Jose: The AAAI Press

[5]

Bolger A M , Lohse M , Usadel B . (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30(15): 2114–2120

[6]

Brown C L , Mullet J , Hindi F , Stoll J E , Gupta S , Choi M , Keenum I , Vikesland P , Pruden A , Zhang L Q . (2022). mobileOG-db: a manually curated database of protein families mediating the life cycle of bacterial mobile genetic elements. Applied and Environmental Microbiology, 88(18): e0099122

[7]

Camargo A P , Roux S , Schulz F , Babinski M , Xu Y , Hu B , Chain P S G , Nayfach S , Kyrpides N C . (2024). Identification of mobile genetic elements with geNomad. Nature Biotechnology, 42(8): 1303–1312

[8]

Chaumeil P A , Mussig A J , Hugenholtz P , Parks D H . (2020). GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics, 36(6): 1925–1927

[9]

del Río Á R , Giner-Lamia J , Cantalapiedra C P , Botas J , Deng Z Q , Hernández-Plaza A , Munar-Palmer M , Santamaría-Hernando S , Rodríguez-Herva J J , Ruscheweyh H J . et al. (2024). Functional and evolutionary significance of unknown genes from uncultivated taxa. Nature, 626(7998): 377–384

[10]

Fan Q S , Zhang J , Shi H R , Chang S H , Hou F J . (2023). Metagenomic profiles of yak and cattle manure resistomes in different feeding patterns before and after composting. Applied and Environmental Microbiology, 89(7): e00645–23

[11]

Fang C , Liu K D , Tian F J , Li J Y , Li S J , Zhang R M , Sun J , Fang L X , Ren H , Wang M G . et al. (2024). Metagenomic analysis unveiled the response of microbial community and antimicrobial resistome in natural water body to duck farm sewage. Environmental Pollution, 361: 124784

[12]

Flórez A B , de los Reyes-Gavilán C G , Wind A , Mayo B , Margolles A . (2006). Ubiquity and diversity of multidrug resistance genes in Lactococcus lactis strains isolated between 1936 and 1995. FEMS Microbiology Letters, 263(1): 21–25

[13]

Guo J R , Bolduc B , Zayed A A , Varsani A , Dominguez-Huerta G , Delmont T O , Pratama A A , Gazitúa M C , Vik D , Sullivan M B . et al. (2021). VirSorter2: a multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome, 9(1): 37

[14]

Guruge S K , Han Z M , Dai S T , Islam A , Ben W , Tian Z , Zhang Y , Yang M . (2025). Seasonal variation of antibiotic resistance genes in activated sludge of a full-scale municipal wastewater treatment plant: contribution of activated sludge functional taxa and clinically relevant taxa. Water Research, 268: 122598

[15]

Johnson M , Zaretskaya I , Raytselis Y , Merezhuk Y , Mcginnis S , Madden T L . (2008). NCBI BLAST: a better web interface. Nucleic Acids Research, 36(S2): W5–W9

[16]

Li D H , Liu C M , Luo R B , Sadakane K , Lam T W . (2015). MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics, 31(10): 1674–1676

[17]

Li Y Z , Zhang S H , Chen Z , Huang W Z , Liu Q , Fang H D , Chi B , Yang N B , Zhang Q . (2024a). Deciphering the impact of organic loading rate and digestate recirculation on the occurrence patterns of antibiotics and antibiotic resistance genes in dry anaerobic digestion of kitchen waste. Water Research, 261: 122005

[18]

Li Z , Guo X X , Liu B X , Huang T , Liu R Y , Liu X C . (2024b). Metagenome sequencing reveals shifts in phage-associated antibiotic resistance genes from influent to effluent in wastewater treatment plants. Water Research, 253: 121289

[19]

Liang C Y , Xie B , Su Y L , Shi J P , Liu L , Zhang S Y . (2025). Mechanistic insights into the attenuation of antibiotic resistance genes in thermophilic anaerobic co-digestion of food waste: a comprehensive metagenomic and absolute quantification study. Chemical Engineering Journal, 505: 159794

[20]

Liu K D , Wang M G , Zhang Y , Fang C , Zhang R M , Fang L X , Sun J , Liu Y H , Liao X P . (2024a). Distribution of antibiotic resistance genes and their pathogen hosts in duck farm environments in south-east coastal China. Applied Microbiology and Biotechnology, 108(1): 136

[21]

Liu Q Q , Jin X J , Cheng J , Zhou H J , Zhang Y J , Dai Y Z . (2023). Advances in the application of molecular diagnostic techniques for the detection of infectious disease pathogens (Review). Molecular Medicine Reports, 27(5): 104

[22]

Liu W , Xu C Y , Li T L , Ren Z R , Hao S , Chen Z , Huang X , Wen X H . (2024b). Temporal dynamics and contribution of phage community to the prevalence of antibiotic resistance genes in a full-scale sludge anaerobic digestion plant. Environmental Science & Technology, 58(14): 6296–6304

[23]

Lu J , Guo J H . (2024). Prophage induction by non-antibiotic compounds promotes transformation of released antibiotic resistance genes from cell lysis. Water Research, 263: 122200

[24]

Mosbæk F , Kjeldal H , Mulat D G , Albertsen M , Ward A J , Feilberg A , Nielsen J L . (2016). Identification of syntrophic acetate-oxidizing bacteria in anaerobic digesters by combined protein-based stable isotope probing and metagenomics. The ISME Journal, 10(10): 2405–2418

[25]

Nayfach S , Camargo A P , Schulz F , Eloe-Fadrosh E , Roux S , Kyrpides N C . (2021). CheckV assesses the quality and completeness of metagenome-assembled viral genomes. Nature Biotechnology, 39(5): 578–585

[26]

Nemeghaire S , Argudín M A , Feßler A T , Hauschild T , Schwarz S , Butaye P . (2014). The ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes. Veterinary Microbiology, 171(3−4): 342–356

[27]

Roux S , Páez-Espino D , Chen I M A , Palaniappan K , Ratner A , Chu K , Reddy T B K , Nayfach S , Schulz F , Call L . et al. (2021). IMG/VR v3: an integrated ecological and evolutionary framework for interrogating genomes of uncultivated viruses. Nucleic Acids Research, 49(D1): D764–D775

[28]

Russel J , Pinilla-Redondo R , Mayo-Muñoz D , Shah S A , Sørensen S J . (2020). CRISPRCasTyper: automated identification, annotation, and classification of CRISPR-cas loci. The CRISPR Journal, 3(6): 462–469

[29]

Shang J Y , Tang X B , Sun Y N . (2023). PhaTYP: predicting the lifestyle for bacteriophages using BERT. Briefings in Bioinformatics, 24(1): bbac487

[30]

Shao Y T , Wang Y P , Yuan Y W , Xie Y J . (2021). A systematic review on antibiotics misuse in livestock and aquaculture and regulation implications in China. Science of the Total Environment, 798: 149205

[31]

Silpe J E , Wong J W H , Owen S V , Baym M , Balskus E P . (2022). The bacterial toxin colibactin triggers prophage induction. Nature, 603(7900): 315–320

[32]

Stogios P J , Savchenko A . (2020). Molecular mechanisms of vancomycin resistance. Protein Science, 29(3): 654–669

[33]

Syafiuddin A , Boopathy R . (2021). Role of anaerobic sludge digestion in handling antibiotic resistant bacteria and antibiotic resistance genes – A review. Bioresource Technology, 330: 124970

[34]

Uritskiy G V , DiRuggiero J , Taylor J . (2018). MetaWRAP-a flexible pipeline for genome-resolved metagenomic data analysis. Microbiome, 6(1): 158

[35]

Volkova V V , Lu Z , Besser T , Gröhn Y T . (2014). Modeling the infection dynamics of bacteriophages in enteric Escherichia coli: estimating the contribution of transduction to antimicrobial gene spread. Applied and Environmental Microbiology, 80(14): 4350–4362

[36]

Walker P J , Siddell S G , Lefkowitz E J , Mushegian A R , Adriaenssens E M , Alfenas-Zerbini P , Dempsey D M , Dutilh B E , García M L , Curtis Hendrickson R . et al. (2022). Recent changes to virus taxonomy ratified by the International Committee on Taxonomy of Viruses (2022). Archives of Virology, 167(11): 2429–2440

[37]

Wang C X , Yin X L , Xu X Q , Wang D , Wang Y B , Zhang T . (2025a). Antibiotic resistance genes in anaerobic digestion: unresolved challenges and potential solutions. Bioresource Technology, 419: 132075

[38]

Wang F , Li Y , Zhang L J , Su Y L , Zhang Y , Hong S , Zhan M , Xie B . (2025b). Biochar alleviates adverse effects of polystyrene microplastics on anaerobic digestion performance of food waste and antibiotic resistance gene propagation. Bioresource Technology, 434: 132771

[39]

Wang S , Hu Y S , Hu Z H , Wu W X , Wang Z Z , Jiang Y , Zhan X M . (2021). Improved reduction of antibiotic resistance genes and mobile genetic elements from biowastes in dry anaerobic co-digestion. Waste Management, 126: 152–162

[40]

Westerholm M , Roos S , Schnürer A . (2011). Tepidanaerobacter acetatoxydans sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from two ammonium-enriched mesophilic methanogenic processes. Systematic and Applied Microbiology, 34(4): 260–266

[41]

Xu M Y , Xu X K , Song Y Y , Xiong J P , Ji Y , Yu B , Liu J G . (2025). Overview and perspectives of sustainable recycling of anaerobic digestion biogas residue of organic solid waste in China. Frontiers of Environmental Science & Engineering, 19(11): 144

[42]

Yin X L , Chen X , Jiang X T , Yang Y , Li B , Shum M H H , Lam T T Y , Leung G M , Rose J , Sanchez-Cid C . et al. (2023). Toward a universal unit for quantification of antibiotic resistance genes in environmental samples. Environmental Science & Technology, 57(26): 9713–9721

[43]

Yin X L , Jiang X T , Chai B L , Li L G , Yang Y , Cole J R , Tiedje J M , Zhang T . (2018). ARGs-OAP v2.0 with an expanded SARG database and Hidden Markov Models for enhancement characterization and quantification of antibiotic resistance genes in environmental metagenomes. Bioinformatics, 34(13): 2263–2270

[44]

Yu P F , Mathieu J , Li M Y , Dai Z Y , Alvarez P J J . (2016). Isolation of polyvalent bacteriophages by sequential multiple-host approaches. Applied and Environmental Microbiology, 82(3): 808–815

[45]

Zhang A N , Gaston J M , Dai C L , Zhao S J , Poyet M , Groussin M , Yin X L , Li L G , van Loosdrecht M C M , Topp E . et al. (2021). An omics-based framework for assessing the health risk of antimicrobial resistance genes. Nature Communications, 12(1): 4765

[46]

Zhang J Y , Lu T D , Song Y P , Rocha U N D , Liu J B , Nikolausz M , Wei Y S , Richnow H H . (2024). Viral communities contribute more to the lysis of antibiotic-resistant bacteria than the transduction of antibiotic resistance genes in anaerobic digestion revealed by metagenomics. Environmental Science & Technology, 58(5): 2346–2359

[47]

Zhang R , Yang S , An Y W , Wang Y Q , Lei Y , Song L Y . (2022a). Antibiotics and antibiotic resistance genes in landfills: a review. Science of the Total Environment, 806: 150647

[48]

Zhang Z H , Li X , Liu H , Zamyadi A , Guo W S , Wen H T , Gao L , Nghiem L D , Wang Q L . (2022b). Advancements in detection and removal of antibiotic resistance genes in sludge digestion: a state-of-art review. Bioresource Technology, 344: 126197

[49]

Zhuang M , Achmon Y , Cao Y P , Liang X M , Chen L , Wang H , Siame B A , Leung K Y . (2021). Distribution of antibiotic resistance genes in the environment. Environmental Pollution, 285: 117402

RIGHTS & PERMISSIONS

Higher Education Press 2026

PDF (4066KB)

Supplementary files

Supplementary materials

1

Accesses

0

Citation

Detail

Sections
Recommended

/