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The Transferable Resistome of Produce.

ABSTRACT: Produce is increasingly recognized as a reservoir of human pathogens and transferable antibiotic resistance genes. This study aimed to explore methods to characterize the transferable resistome of bacteria associated with produce. Mixed salad, arugula, and cilantro purchased from supermarkets in Germany were analyzed by means of cultivation- and DNA-based methods. Before and after a nonselective enrichment step, tetracycline (TET)-resistant Escherichia coli were isolated and plasmids conferring TET resistance were captured by exogenous plasmid isolation. TET-resistant E. coli isolates, transconjugants, and total community DNA (TC-DNA) from the microbial fraction detached from leaves or after enrichment were analyzed for the presence of resistance genes, class 1 integrons, and various plasmids by real-time PCR and PCR-Southern blot hybridization. Real-time PCR primers were developed for IncI and IncF plasmids. TET-resistant E. coli isolated from arugula and cilantro carried IncF, IncI1, IncN, IncHI1, IncU, and IncX1 plasmids. Three isolates from cilantro were positive for IncN plasmids and bla CTX-M-1 From mixed salad and cilantro, IncF, IncI1, and IncP-1? plasmids were captured exogenously. Importantly, whereas direct detection of IncI and IncF plasmids in TC-DNA failed, these plasmids became detectable in DNA extracted from enrichment cultures. This confirms that cultivation-independent DNA-based methods are not always sufficiently sensitive to detect the transferable resistome in the rare microbiome. In summary, this study showed that an impressive diversity of self-transmissible multiple resistance plasmids was detected in bacteria associated with produce that is consumed raw, and exogenous capturing into E. coli suggests that they could transfer to gut bacteria as well.IMPORTANCE Produce is one of the most popular food commodities. Unfortunately, leafy greens can be a reservoir of transferable antibiotic resistance genes. We found that IncF and IncI plasmids were the most prevalent plasmid types in E. coli isolates from produce. This study highlights the importance of the rare microbiome associated with produce as a source of antibiotic resistance genes that might escape cultivation-independent detection, yet may be transferred to human pathogens or commensals.

SUBMITTER: Blau K

PROVIDER: S-EPMC6222124 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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The Transferable Resistome of Produce.

Blau Khald K Bettermann Antje A Jechalke Sven S Fornefeld Eva E Vanrobaeys Yann Y Stalder Thibault T Top Eva M EM Smalla Kornelia K

mBio 20181106 6

Produce is increasingly recognized as a reservoir of human pathogens and transferable antibiotic resistance genes. This study aimed to explore methods to characterize the transferable resistome of bacteria associated with produce. Mixed salad, arugula, and cilantro purchased from supermarkets in Germany were analyzed by means of cultivation- and DNA-based methods. Before and after a nonselective enrichment step, tetracycline (TET)-resistant <i>Escherichia coli</i> were isolated and plasmids conf ...[more]

PMID: 30401772

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Project description:Methicillin-resistant Staphylococcus sciuri (MRSS) strain C2865 from a stranded dog in Nigeria was trimethoprim (TMP) resistant but lacked formerly described staphylococcal TMP-resistant dihydrofolate reductase genes (dfr). Whole-genome sequencing, comparative genomics, and pan-genome analyses were pursued to unveil the molecular bases for TMP resistance via resistome and mobilome profiling. MRSS C2865 comprised a species subcluster and positioned just above the intraspecies boundary. Lack of species host tropism was observed. S. sciuri exhibited an open pan-genome, while MRSS C2865 harbored the highest number of unique genes (75% associated with mobilome). Within this fraction, we discovered a transferable TMP resistance gene, named dfrE, which confers high-level TMP resistance in Staphylococcus aureus and Escherichia coli. dfrE was located in a novel multidrug resistance mosaic plasmid (pUR2865-34) encompassing adaptive, mobilization, and segregational stability traits. dfrE was formerly denoted as dfr_like in Exiguobacterium spp. from fish farm sediment in China but escaped identification in one macrococcal and diverse staphylococcal genomes in different Asian countries. dfrE shares the highest identity with dfr of soil-related Paenibacillus anaericanus (68%). Data analysis discloses that dfrE has emerged from a single ancestor and places S. sciuri as a plausible donor. C2865 unique fraction additionally enclosed novel chromosomal mobile islands, including a multidrug-resistant pseudo-SCCmec cassette, three apparently functional prophages (Siphoviridae), and an SaPI4-related staphylococcal pathogenicity island. Since dfrE seems not yet common in staphylococcal clinical specimens, our data promote early surveillance and enable molecular diagnosis. We evidence the genome plasticity of S. sciuri and highlight its role as a resourceful reservoir for adaptive traits. IMPORTANCE The discovery and surveillance of antimicrobial resistance genes (AMRG) and their mobilization platforms are critical to understand the evolution of bacterial resistance and to restrain further expansion. Limited genomic data are available on Staphylococcus sciuri; regardless, it is considered a reservoir for critical AMRG and mobile elements. We uncover a transferable staphylococcal TMP resistance gene, named dfrE, in a novel mosaic plasmid harboring additional resistance, adaptive, and self-stabilization features. dfrE is present but evaded detection in diverse species from varied sources geographically distant. Our analyses evidence that the dfrE-carrying element has emerged from a single ancestor and position S. sciuri as the donor species for dfrE spread. We also identify novel mobilizable chromosomal islands encompassing AMRG and three unrelated prophages. We prove high intraspecies heterogenicity and genome plasticity for S. sciuri. This work highlights the importance of genome-wide ecological studies to facilitate identification, characterization, and evolution routes of bacteria adaptive features.

Dataset Information

The Transferable Resistome of Produce.

Publications

The Transferable Resistome of Produce.

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