Mobilization of Antibiotic Resistance: Are Current Approaches for Colocalizing Resistomes and Mobilomes Useful?

Slizovskiy, Ilya B.; Mukherjee, Kingshuk; Dean, Christopher; Boucher, Christina; Noyes, Noelle

doi:10.3389/fmicb.2020.01376

Cited by 40 publications

(42 citation statements)

References 110 publications

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“…Finally, it is acknowledged that metagenomic analysis is an evolving field, particularly for the characterization of antibiotic resistance in complex environmental samples [51,81,82]. Here we demonstrated that overall Fig.…”

Section: Discussionsupporting

confidence: 59%

“…ARGs were annotated against the Comprehensive Antibiotic Resistance Database (CARD v1.0.6) [49] and plasmid-associated genes against the ACLAME database [50]. Given that differing annotation parameters and databases could produce different trends [51], resistomes of all samples were also annotated with DeepARG, which incorporates several publicly available databases and uses a deep learning algorithm to maximize ARG detection [47]. Relative abundances of total ARGs predicted by DeepARG were found to be strongly and significantly correlated with those annotated using CARD via MetaStorm, as described above (Fig.…”

Section: Metagenomic Sequencing and Analysismentioning

confidence: 99%

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Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes

et al. 2021

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Background Research 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. Results Progression 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. Conclusions This 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.

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Section: Discussionsupporting

confidence: 59%

Section: Metagenomic Sequencing and Analysismentioning

confidence: 99%

Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes

et al. 2021

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“…(2) These ARGs might be available at an undetected level before the treatment; however, danofloxacin administration might have favored horizontal gene transfer among genetically related and, probably, unrelated bacteria. Horizontal gene transfer is a common way of acquiring ARGs by bacteria in complex environments, such as in the gut [27,68,69]. Co-transfer of ermB and tetM in Streptococcus pyogenes was reported, which suggested their linkage in individual genetic elements [70].…”

Section: Discussionmentioning

confidence: 99%

Danofloxacin Treatment Alters the Diversity and Resistome Profile of Gut Microbiota in Calves

et al. 2021

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Fluoroquinolones, such as danofloxacin, are used to control bovine respiratory disease complex in beef cattle; however, little is known about their effects on gut microbiota and resistome. The objectives were to evaluate the effect of subcutaneously administered danofloxacin on gut microbiota and resistome, and the composition of Campylobacter in calves. Twenty calves were injected with a single dose of danofloxacin, and ten calves were kept as a control. The effects of danofloxacin on microbiota and the resistome were assessed using 16S rRNA sequencing, quantitative real-time PCR, and metagenomic Hi-C ProxiMeta. Alpha and beta diversities were significantly different (p < 0.05) between pre-and post-treatment samples, and the compositions of several bacterial taxa shifted. The patterns of association between the compositions of Campylobacter and other genera were affected by danofloxacin. Antimicrobial resistance genes (ARGs) conferring resistance to five antibiotics were identified with their respective reservoirs. Following the treatment, some ARGs (e.g., ant9, tet40, tetW) increased in frequencies and host ranges, suggesting initiation of horizontal gene transfer, and new ARGs (aac6, ermF, tetL, tetX) were detected in the post-treatment samples. In conclusion, danofloxacin induced alterations of gut microbiota and selection and enrichment of resistance genes even against antibiotics that are unrelated to danofloxacin.

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“…The finding that the secondary effluent samples have higher mobilome diversity and composition does not immediately increase the potential of clinically relevant transfer risks to receiving environments, as these will be related to associations with AMR elements. Clearly significant numbers of resistome genes are either in plasmid-derived sequences or are associated with other mobile genetic elements, with implications for mobilization of antimicrobial resistance (Slizovskiy et al 2020).…”

Section: Effect Of Wastewater Treatment On the Resistome And Mobilomementioning

confidence: 99%

Nanopore-based metagenomics analysis reveals prevalence of mobile antibiotic and heavy metal resistome in wastewater

Martin¹,

Stebbins

Ajmani

et al. 2021

Ecotoxicology

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In-depth studies of the microbiome and mobile resistome profile of different environments is central to understanding the role of the environment in antimicrobial resistance (AMR), which is one of the urgent threats to global public health. In this study, we demonstrated the use of a rapid (and easily portable) sequencing approach coupled with user-friendly bioinformatics tools, the MinION (Oxford Nanopore Technologies), on the evaluation of the microbial as well as mobile metal and antibiotic resistome profile of semi-rural wastewater. A total of 20 unique phyla, 43 classes, 227 genera, and 469 species were identified in samples collected from the Amherst Wastewater Treatment Plant, both from primary and secondary treated wastewater. Alpha diversity indices indicated that primary samples were significantly richer and more microbially diverse than secondary samples. A total of 1041 ARGs, 68 MRGs, and 17 MGEs were detected in this study. There were more classes of AMR genes in primary than secondary wastewater, but in both cases multidrug, beta-lactam and peptide AMR predominated. Of note, OXA β-lactamases, some of which are also carbapenemases, were enriched in secondary samples. Metal resistance genes against arsenic, copper, zinc and molybdenum were the dominant MRGs in the majority of the samples. A larger proportion of resistome genes were located in chromosome-derived sequences except for mobilome genes, which were predominantly located in plasmid-derived sequences. Genetic elements related to transposase were the most common MGEs in all samples. Mobile or MGE/plasmid-associated resistome genes that confer resistance to last resort antimicrobials such as carbapenems and colistin were detected in most samples. Worryingly, several of these potentially transferable genes were found to be carried by clinically-relevant hosts including pathogenic bacterial species in the orders Aeromonadales, Clostridiales, Enterobacterales and Pseudomonadales. This study demonstrated that the MinION can be used as a metagenomics approach to evaluate the microbiome, resistome, and mobilome profile of primary and secondary wastewater.

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Mobilization of Antibiotic Resistance: Are Current Approaches for Colocalizing Resistomes and Mobilomes Useful?

Cited by 40 publications

References 110 publications

Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes

Combined effects of composting and antibiotic administration on cattle manure–borne antibiotic resistance genes

Danofloxacin Treatment Alters the Diversity and Resistome Profile of Gut Microbiota in Calves

Nanopore-based metagenomics analysis reveals prevalence of mobile antibiotic and heavy metal resistome in wastewater

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