Dataset Information

Viral and thermal lysis facilitates transmission of antibiotic resistance genes during composting.

ABSTRACT: While the distribution of extracellular ARGs (eARGs) in the environment has been widely reported, the factors governing their release remain poorly understood. Here, we combined multi-omics and direct experimentation to test whether the release and transmission of eARGs are associated with viral lysis and heat during cow manure composting. Our results reveal that the proportion of eARGs increased 2.7-fold during composting, despite a significant and concomitant reduction in intracellular ARG abundances. This relative increase of eARGs was driven by composting temperature and viral lysis of ARG-carrying bacteria based on metagenome-assembled genome (MAG) analysis. Notably, thermal lysis of mesophilic bacteria carrying ARGs was a key factor in releasing eARGs at the thermophilic phase, while viral lysis played a relatively stronger role during the non-thermal phase of composting. Furthermore, MAG-based tracking of ARGs in combination with direct transformation experiments demonstrated that eARGs released during composting pose a potential transmission risk. Our study provides bioinformatic and experimental evidence of the undiscovered role of temperature and viral lysis in co-driving the spread of ARGs in compost microbiomes via the horizontal transfer of environmentally released DNA.

Importance

The spread of antibiotic resistance genes (ARGs) is a critical global health concern. Understanding the factors influencing the release of extracellular ARGs (eARGs) is essential for developing effective strategies. In this study, we investigated the association between viral lysis, heat, and eARG release during composting. Our findings revealed a substantial increase in eARGs despite reduced intracellular ARG abundance. Composting temperature and viral lysis were identified as key drivers, with thermal lysis predominant during the thermophilic phase and viral lysis during non-thermal phases. Moreover, eARGs released during composting posed a transmission risk through horizontal gene transfer. This study highlights the significance of temperature and phage lysis in ARG spread, providing valuable insights for mitigating antibiotic resistance threats.

SUBMITTER: Ai C

PROVIDER: S-EPMC11337816 | biostudies-literature | 2024 Jul

REPOSITORIES: biostudies-literature

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Viral and thermal lysis facilitates transmission of antibiotic resistance genes during composting.

Ai Chaofan C Cui Peng P Liu Chen C Wu Jiawei J Xu Yuan Y Liang Xiaolong X Yang Qiu-E Q Tang Xiang X Zhou Shungui S Liao Hanpeng H Friman Ville-Petri V-P

Applied and environmental microbiology 20240730 8

While the distribution of extracellular ARGs (eARGs) in the environment has been widely reported, the factors governing their release remain poorly understood. Here, we combined multi-omics and direct experimentation to test whether the release and transmission of eARGs are associated with viral lysis and heat during cow manure composting. Our results reveal that the proportion of eARGs increased 2.7-fold during composting, despite a significant and concomitant reduction in intracellular ARG abu ...[more]

PMID: 39078126

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Project description:BackgroundResearch is needed to delineate the relative and combined effects of different antibiotic administration and manure management practices in either amplifying or attenuating the potential for antibiotic resistance to spread. Here, we carried out a comprehensive parallel examination of the effects of small-scale (> 55 °C × 3 days) static and turned composting of manures from dairy and beef cattle collected during standard antibiotic administration (cephapirin/pirlimycin or sulfamethazine/chlortetracycline/tylosin, respectively), versus from untreated cattle, on "resistomes" (total antibiotic resistance genes (ARGs) determined via shotgun metagenomic sequencing), bacterial microbiota, and indicator ARGs enumerated via quantitative polymerase chain reaction. To gain insight into the role of the thermophilic phase, compost was also externally heated to > 55 °C × 15 days.ResultsProgression of composting with time and succession of the corresponding bacterial microbiota was the overarching driver of the resistome composition (ANOSIM; R = 0.424, p = 0.001, respectively) in all composts at the small-scale. Reduction in relative abundance (16S rRNA gene normalized) of total ARGs in finished compost (day 42) versus day 0 was noted across all conditions (ANOSIM; R = 0.728, p = 0.001), except when externally heated. Sul1, intI1, beta-lactam ARGs, and plasmid-associated genes increased in all finished composts as compared with the initial condition. External heating more effectively reduced certain clinically relevant ARGs (blaOXA, blaCARB), fecal coliforms, and resistome risk scores, which take into account putative pathogen annotations. When manure was collected during antibiotic administration, taxonomic composition of the compost was distinct according to nonmetric multidimensional analysis and tet(W) decayed faster in the dairy manure with antibiotic condition and slower in the beef manure with antibiotic condition.ConclusionsThis comprehensive, integrated study revealed that composting had a dominant effect on corresponding resistome composition, while little difference was noted as a function of collecting manure during antibiotic administration. Reduction in total ARGs, tet(W), and resistome risk suggested that composting reduced some potential for antibiotic resistance to spread, but the increase and persistence of other indicators of antibiotic resistance were concerning. Results indicate that composting guidelines intended for pathogen reduction do not necessarily provide a comprehensive barrier to ARGs or their mobility prior to land application and additional mitigation measures should be considered. Video Abstract.

Project description:Pig manure is a reservoir of antibiotics and antibiotic resistance genes (ARGs). The effect of biochar on the variations in physicochemical properties, bacterial communities, antibiotics, ARGs, and mobile genetic elements (MGEs) of compost product during co-composting of pig manure and corn straw have been investigated in this study. Compared with the control treatment (CK), biochar addition accelerated the increase in pile temperature and prolonged the high temperature period (>55°C) for 2 days. Under biochar influence, organic matter degradation, NH4 +-N conversion and NO3 --N production was accelerated, and dissolved total organic carbon (DOC) and dissolved total nitrogen (DTN) utilization by microorganisms were enhanced. Biochar addition altered the microbial community and promoted the vital activity of Actinobacteria in the later composting stage. The antibiotics removal efficiency (except danofloxacin and enrofloxacin) was accelerated in the early composting stage (1-14 days) by biochar addition, the pile temperature had a positive effect on antibiotics removal, and the total antibiotics removal efficiency in CK and CK+Biochar treatments was 69.58% and 78.67% at the end of the composting process, respectively. The absolute abundance of most of the ARGs in the CK+Biochar treatment was lower than that in the CK treatment during composting, and the ARGs removal mainly occurred in the early (1-14 days) and later (28-50 days) stages. Biochar addition reduced the absolute abundance of MGEs (intI1, intI2) in the compost product, and most of the ARGs had a significant positive correlation with MGEs. Network analysis and redundancy analysis showed that ARGs and MGEs occurred in various host bacteria (Firmicutes, Actinobacteria, Bacteroidetes, Proteobacteria, and Halanaerobiaeota), and that DTN and NH4 +-N are the main factors regulating the changes in bacterial communities, antibiotics, ARGs, and MGEs during composting. Moreover, MGEs contributed the most to the variation in ARGs. In summary, biochar addition during composting accelerated antibiotics removal and inhibited accumulation and transmission of ARGs. The results of this study could provide theoretical and technical support for biochar application for antibiotics and ARGs removal during livestock and poultry manure composting.

Project description:Organic fertilizer is a major carrier that stores and transmits antibiotic resistance genes (ARGs). In the environment, due to the application of organic fertilizers in agriculture, the increasing diversity and abundance of ARGs poses a potential threat to human health and environmental safety. In this paper, the microbial community structure and ARGs in different types of organic fertilizer treated with composting were examined. We found that the abundance and diversity of ARGs in earthworm cast organic fertilizer were the lowest and the highest in chicken manure organic fertilizer. Interestingly, the abundance and diversity of ARGs, especially beta-lactam resistance genes, sulfonamide resistance genes, and macrolide-lincosamide-streptogramin B (MLSB) resistance genes, in organic fertilizers were reduced significantly, while composting caused no significant change in mobile genetic elements (MGEs), where antibiotic deactivation and the use of efflux pumps were the two most dominant mechanisms. It was clear that removal of ARGs became more efficient with increasing reduction in the bacterial abundances and diversity of potential ARG hosts, and integron-mediated horizontal gene transfers (HGTs) played an important role in the proliferation of most ARG types. Therefore, the reduction in ARGs was mainly driven by changes in bacterial community composition caused by composting. Furthermore, rather than HGTs, the diversity and abundance of bacterial communities affected by compost physical and chemical properties were the main drivers shaping and altering the abundance and diversity of ARGs, which was indicated by a correlation analysis of these properties, antibiotic residues, microbial community structure, and ARGs. In general, high-temperature composting effectively removed antibiotic residues and ARGs from these organic fertilizers; however, it cannot prevent the proliferation of MGEs. The insights gained from these results may be of assistance in the safe and rational use of organic fertilizers by indicating the changes in microbial community structure and ARGs in different types of organic fertilizer treated with composting.

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Viral and thermal lysis facilitates transmission of antibiotic resistance genes during composting.

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Viral and thermal lysis facilitates transmission of antibiotic resistance genes during composting.

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