The Shared Antibiotic Resistome of Soil Bacteria and Human Pathogens

Forsberg, Kevin J.; Reyes, Alejandro; Wang, Bin; Selleck, Elizabeth M.; Sommer, Morten Otto Alexander; Dantas, Gautam

doi:10.1126/science.1220761

Cited by 1,390 publications

(981 citation statements)

References 37 publications

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“…In this study MGEs explained only 4.1% variation of ARGs. It has been suggested that it is the phylogeny, rather than HGT as the primary determinant of soil resistome content (Forsberg et al, 2012;Forsberg et al, 2014). Therefore, as bacterial diversity changes across soils, so do their associated ARGs, resulting in resistome that may respond to anthropogenic modulations that even do not possess obvious antibiotic-related properties (such as chemical fertilizer).…”

Section: Linkages Between Bacterial Community and Antibiotic Resistomementioning

confidence: 99%

Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil

Chen

et al. 2016

Environment International

685

246

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Section: Linkages Between Bacterial Community and Antibiotic Resistomementioning

confidence: 99%

Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil

Chen

et al. 2016

Environment International

685

246

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“…In recent EAHEC outbreaks in Germany, recombination of a pathogenic with the plasmid of a non-pathogenic E. coli strain increased the pathogenic potential to cause a deadly combination (Brzuszkiewicz et al, 2011). Soil-borne antibiotic resistance has been found to be shared with human pathogens (Benveniste and Davies, 1973;Forsberg et al, 2012). Several organisms among the identified transconjugants belong to groups known to contain opportunistic human pathogens, providing a direct link between the plasmid encoded mobile soil resistome and opportunistic pathogens.…”

Section: Medical Relevancementioning

confidence: 99%

“…Horizontal gene transfer between different species has been recognized as a common and major evolutionary process (Zhaxybayeva and Doolittle, 2011), most acutely demonstrated in the heavy interconnection between the resistome of soil dwelling bacteria and human pathogens (Forsberg et al, 2012). The behavior of this environmental resistome may, thus, govern the spread of antibiotic resistance genes to pathogens (Finley et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community

et al. 2014

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Conjugal plasmids can provide microbes with full complements of new genes and constitute potent vehicles for horizontal gene transfer. Conjugal plasmid transfer is deemed responsible for the rapid spread of antibiotic resistance among microbes. While broad host range plasmids are known to transfer to diverse hosts in pure culture, the extent of their ability to transfer in the complex bacterial communities present in most habitats has not been comprehensively studied. Here, we isolated and characterized transconjugants with a degree of sensitivity not previously realized to investigate the transfer range of IncP-and IncPromA-type broad host range plasmids from three proteobacterial donors to a soil bacterial community. We identified transfer to many different recipients belonging to 11 different bacterial phyla. The prevalence of transconjugants belonging to diverse Gram-positive Firmicutes and Actinobacteria suggests that inter-Gram plasmid transfer of IncP-1 and IncPromAtype plasmids is a frequent phenomenon. While the plasmid receiving fractions of the community were both plasmid-and donor-dependent, we identified a core super-permissive fraction that could take up different plasmids from diverse donor strains. This fraction, comprising 80% of the identified transconjugants, thus has the potential to dominate IncP-and IncPromA-type plasmid transfer in soil. Our results demonstrate that these broad host range plasmids have a hitherto unrecognized potential to transfer readily to very diverse bacteria and can, therefore, directly connect large proportions of the soil bacterial gene pool. This finding reinforces the evolutionary and medical significances of these plasmids.

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“…Therefore, ARGs have been recognized as an important environmental contaminant of global concern (Pruden et al 2006). Along with the rising burdens of ARGs, it was reported that environmental ARGs could directly transfer from environments to humans, through their persisting and spreading in the environment and subsequent dissemination into the food chain (Forsberg et al 2012;Zhu et al 2013). Furthermore, the transfer of ARGs from environmental bacteria to human-associated pathogens could be facilitated through mobility elements such as integrons, plasmids and transposons (Gogartion and Townsend 2005;Binh et al 2008).…”

Section: Introductionmentioning

confidence: 99%

“…As the only ecosystem interacting constantly with all compartments of the biosphere, soil is prone to genetic exchange by means of horizontal gene transfer between ecologically distinct lineages found in other ecosystems (Nesme and Simonet 2014). High-throughput functional metagenomic analysis found that soil bacteria harbor resistance gene cassettes against all major classes of antibiotics with high similarity to genes from human pathogens (Forsberg et al 2012). The spread and aggregation of ARGs in soil environments have been strongly correlated with intensive antibiotic use by an extensive body of studies (Binh et al 2008;Heuer, Schmitt and Smalla 2011a), and might have been accelerated by anthropogenic activities such as agricultural practices, animal husbandry and manure application (Allen et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Temporal changes of antibiotic-resistance genes and bacterial communities in two contrasting soils treated with cattle manure

Han

Shi

et al. 2015

FEMS Microbiology Ecology

111

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One sentence summary: The study indicates that even in the absence of selective pressure imposed by agricultural use of antibiotics, manure application could still strongly impact the abundance, diversity and mobility potential of a broad spectrum of soil ARGs. Editor: Kornelia Smalla ABSTRACTThe emerging environmental spread of antibiotic-resistance genes (ARGs) and their subsequent acquisition by clinically relevant microorganisms is a major threat to public health. Animal manure has been recognized as an important reservoir of ARGs; however, the dissemination of manure-derived ARGs and the impacts of manure application on the soil resistome remain obscure. Here, we conducted a microcosm study to assess the temporal succession of total bacteria and a broad spectrum of ARGs in two contrasting soils following manure application from cattle that had not been treated with antibiotics. High-capacity quantitative PCR detected 52 unique ARGs across all the samples, with β-lactamase as the most dominant ARG type. Several genes of soil indigenous bacteria conferring resistance to β-lactam, which could not be detected in manure, were found to be highly enriched in manure-treated soils, and the level of enrichment was maintained over the entire course of 140 days. The enriched β-lactam resistance genes had significantly positive relationships with the relative abundance of the integrase intI1 gene, suggesting an increasing mobility potential in manure-treated soils. The changes in ARG patterns were accompanied by a significant effect of cattle manure on the total bacterial community compositions. Our study indicates that even in the absence of selective pressure imposed by agricultural use of antibiotics, manure application could still strongly impact the abundance, diversity and mobility potential of a broad spectrum of soil ARGs. Our findings are important for reliable prediction of ARG behaviors in soil environment and development of appropriate strategies to minimize their dissemination.

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The Shared Antibiotic Resistome of Soil Bacteria and Human Pathogens

Cited by 1,390 publications

References 37 publications

Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil

Long-term field application of sewage sludge increases the abundance of antibiotic resistance genes in soil

Broad host range plasmids can invade an unexpectedly diverse fraction of a soil bacterial community

Temporal changes of antibiotic-resistance genes and bacterial communities in two contrasting soils treated with cattle manure

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