Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter

Nandi, Sobhan; Maurer, John J.; Hofacre, Charles L.; Summers, Anne O.

doi:10.1073/pnas.0306466101

Cited by 261 publications

(197 citation statements)

References 52 publications

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“…Especially, IncP1e plasmids such as pKJK5 have been identified as vectors of antibiotic resistance genes transfer among Proteobacteria by additionally hosting class 1 integron gene cassettes (Heuer et al, 2012). These class 1 integrons may not only spread in their originally identified Gram-negative Enterobacteriaceae hosts but can also be found among many Gram-positive bacteria (Nandi et al, 2004). Here, we demonstrated a possible direct way of accession of these class 1 integrons in Gram-positive bacteria through IncP-1e plasmid transfer from Proteobacteria.…”

Section: Medical Relevancementioning

confidence: 78%

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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Section: Medical Relevancementioning

confidence: 78%

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

et al. 2014

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“…Regardless of variance within Beaver Dam Creek, intI1 was consistently more abundant across multiple microhabitats in comparison with the reference site, Meyers Branch. Culture-based and molecular estimates of intI1 abundance in bacteria of environmental origin indicate that between 1% and 10% of bacteria possess these genes (C Baker-Austin, unpublished data; Nandi et al, 2004;Boucher et al, 2007), although Biyela et al (2004) found class 1 integrons in over 50% of isolates with multiple drug resistances from an urban South African river. Variation in the proportion of a bacterial community possessing class 1 integrons outside of clinical settings is likely to be the result of several factors including (1) distance to an enriched source of class 1 integrons (for example, sewage treatment plant); (2) integron dispersal ability (for example, mobilization of the integron via physical linkage to a plasmid or transposon); (3) the taxonomic composition of the community; (4) horizontal gene transfer potential in a given habitat; and (5) intensity of selective pressure favoring the maintenance of genes contained within the integron.…”

Section: Discussionmentioning

confidence: 99%

“…Several studies have detected MGEs including plasmids, transposons and integrons across a wide variety of habitats (for example, Sobecky, 1999;Smalla and Sobecky, 2002;van Elsas and Bailey, 2002;Frost et al, 2005), but rarely in a quantitative manner due to previous methodological constraints. In those studies that did quantify MGE abundance in bacterial communities, class 1 integrase (intI1) genes were shown to be abundant in Gram-positive and Gram-negative bacteria in poultry litter obtained from farms with varying antibiotic usage regimes regardless of antibiotic usage (Nandi et al, 2004), while mercury exposure was recently demonstrated to increase the abundance of IncP-1 plasmids (Smalla et al, 2006). Yet, how MGE abundance is affected by environmental conditions and selective pressures is poorly understood and remains to be tested systematically.…”

Section: Introductionmentioning

confidence: 99%

“…These are independently mobilizable genetic units that normally consist of a single ORF and a cassette-associated recombination site designated a 59-base element or attC. Class 1 integrons were first identified due to their role in the dissemination of antibiotic resistance gene cassettes in clinical bacteria (Stokes and Hall, 1989), but have since been found in a phylogenetically broad range of clinical and environmental bacteria including Gram-negative and Gram-positive bacteria (Nandi et al, 2004;Stokes et al, 2006;Boucher et al, 2007). Environmental surveys of integron-associated gene cassettes indicate that the majority of cassettes include novel sequences unrelated to known antibiotic resistance genes (Stokes et al, 2001;Holmes et al, 2003), with one conservative estimate of cassette richness being at least 2343 different gene cassettes in a 50-m 2 sediment plot (Michael et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

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Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities

et al. 2008

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The acquisition of new genetic material via horizontal gene transfer allows bacteria to rapidly evolve. One key to estimating the contribution of horizontal gene transfer to bacterial evolution is to quantify the abundance of mobile genetic elements (MGEs) in bacterial communities under varying degrees of selective pressure. We quantified class 1 integrase (intI1) gene abundance in total community DNA extracted from contaminated and reference riverine and estuarine microhabitats, and in metal-or antibiotic-amended freshwater microcosms. The intI1 gene was more abundant in all contaminant-exposed communities indicating that relative gene transfer potential is higher in these communities. A second key to assessing the contributions of MGEs to bacterial evolution is to examine the structure and function of the MGE-associated gene pool. We determined that the gene cassette pool is a novel and diverse resource available for bacterial acquisition, but that contamination has no discernible effect on cassette richness. Gene cassette profiles were more similar within sites than among sites, yet bacterial community profiles were not, suggesting that selective pressures can shape the structure of the gene cassette pool. Of the 46 sequenced gene cassette products, 37 were novel sequences, while the 9 gene cassettes with similarity to database sequences were primarily to hypothetical proteins. That class 1 integrons are ubiquitous and abundant in environmental bacterial communities indicates that this group of MGEs can play a substantial role in the acquisition of a diverse array of gene cassettes beyond their demonstrated impact in mediating multidrug resistance in clinical bacteria.

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“…28,30 The use of community DNA from a sample as a means for detecting antibiotic resistance genes and for identifying potential gene reservoirs is becoming more common. 1,27 However, little work has been done on the validation of this approach. The objective of the study reported here was to determine the specific level at which antibiotic resistance genes can be detected within community DNA prepared from cattle fecal samples.…”

Section: Introductionmentioning

confidence: 99%

Development of a Polymerase Chain Reaction Assay for the Detection of Antibiotic Resistance Genes in Community DNA

Patterson

Singer

2006

J VET Diagn Invest

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Abstract. Many methods are used to detect antibiotic resistance genes in samples. The objective of the study reported here was to compare polymerase chain reaction (PCR) analysis of community DNA with fecal culturing for detecting antibiotic resistance genes in cattle samples. In the laboratory-based portion of this study, known concentrations of an Escherichia coli strain with 3 antibiotic resistance genes (cmy-2, flo, and cat) were added to feces from dairy cattle. These genes were used to assess the effect of various primer pairs, chromosomally versus plasmid-encoded genes, and gene copy number on the sensitivity of PCR amplification. Gene-specific PCR amplification was performed on the community DNA extracted from the feces. Feces were cultured for the inoculated strain. In the field-based portion of the study, 80 cattle fecal samples of unknown gene status were compared by use of similar methods. Culture and PCR amplification from community DNA extractions produced variable results, and this variability was most noticeable at dilutions that approached the detection limit of the assay. Typically, PCR amplification had a higher sensitivity than did culture for detecting the gene of interest. However, the sensitivity of culture was improved by plating on selective media containing antibiotics. The community DNA approach enables assessment of bacterial communities in complex samples such as feces, a task that can be prohibitive by budget or time constraints associated with culture methods. Through a strategic combination of culture and community DNA approaches, the relationship between specific selection pressures and the persistence and dissemination of specific resistance genes can be elucidated.

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Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter

Cited by 261 publications

References 52 publications

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

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

Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities

Development of a Polymerase Chain Reaction Assay for the Detection of Antibiotic Resistance Genes in Community DNA

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