Mitigation of antibiotic resistome in swine manure by black soldier fly larval conversion combined with composting

• Published in: The Science of the total environment 2023-06, Vol.879, p.163065-163065, Article 163065
• Main Authors: Zhao, Zhengzheng, Yu, Chan, Yang, Chongrui, Gao, Bingqi, Jiménez, Núria, Wang, Chen, Li, Fang, Ao, Yue, Zheng, Longyu, Huang, Feng, Tomberlin, Jeffery K., Ren, Zhuqing, Yu, Ziniu, Zhang, Jibin, Cai, Minmin
• Format: Article
• Language: English
• Subjects: Animals; Anti-Bacterial Agents - pharmacology; Antibiotic resistance genes; Antibiotic resistant bacteria; Antibiotic-resistant pathogenic bacteria; Antibiotics; Bacteria - genetics; Black soldier fly; Composting; Diptera; Genes, Bacterial; Humans; Larva; Manure - microbiology; Nutrient modification; Swine
• ISSN: 0048-9697; 1879-1026
• DOI: 10.1016/j.scitotenv.2023.163065

The increasing prevalence of antibiotic resistance genes (ARGs) in animal manure has attracted considerable attention because of their potential contribution to the development of multidrug resistance worldwide. Insect technology may be a promising alternative for the rapid attenuation of ARGs in manure; however, the underlying mechanism remains unclear. This study aimed to evaluate the effects of black soldier fly (BSF, Hermetia illucens [L.]) larvae conversion combined with composting on ARGs dynamics in swine manure and to uncover the mechanisms through metagenomic analysis. Compared to natural composting (i.e. without BSF), BSFL conversion combined with composting reduced the absolute abundance of ARGs by 93.2 % within 28 days. The rapid degradation of antibiotics and nutrient reformulation during BSFL conversion combined with composting indirectly altered manure bacterial communities, resulting in a lower abundance and richness of ARGs. The number of main antibiotic-resistant bacteria (e.g., Prevotella, Ruminococcus) decreased by 74.9 %, while their potential antagonistic bacteria (e.g., Bacillus, Pseudomonas) increased by 128.7 %. The number of antibiotic-resistant pathogenic bacteria (e.g., Selenomonas, Paenalcaligenes) decreased by 88.3 %, and the average number of ARGs carried by each human pathogenic bacterial genus declined by 55.8 %. BSF larvae gut microbiota (e.g., Clostridium butyricum, C. bornimense) could help reduce the risk of multidrug-resistant pathogens. These results provide insight into a novel approach to mitigate multidrug resistance from the animal industry in the environment by using insect technology combined with composting, in particular in light of the global “One Health” requirements. [Display omitted] •BSFL reduced ARGs, ARB, and ARPB by 93.2 %, 74.9 %, and 85.6 %, respectively.•BSFL alleviated the risk of ARGs spreading to human pathogenic bacteria.•BSFL gut probiotics reduced the occurrence risk of multidrug resistant pathogens.•BSFL rapidly degraded antibiotics and reformulated nutrient profiles of manure.•Reformed environment indirectly altered bacterial community succession to low ARGs.