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Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera.

ABSTRACT: Antibiotic resistance is a worldwide public health concern. Conjugative transfer between closely related strains or species of bacteria is an important method for the horizontal transfer of multidrug-resistance genes. The extent to which nanomaterials are able to cause an increase in antibiotic resistance by the regulation of the conjugative transfer of antibiotic-resistance genes in bacteria, especially across genera, is still unknown. Here we show that nanomaterials in water can significantly promote the horizontal conjugative transfer of multidrug-resistance genes mediated by the RP4, RK2, and pCF10 plasmids. Nanoalumina can promote the conjugative transfer of the RP4 plasmid from Escherichia coli to Salmonella spp. by up to 200-fold compared with untreated cells. We also explored the mechanisms behind this phenomenon and demonstrate that nanoalumina is able to induce oxidative stress, damage bacterial cell membranes, enhance the expression of mating pair formation genes and DNA transfer and replication genes, and depress the expression of global regulatory genes that regulate the conjugative transfer of RP4. These findings are important in assessing the risk of nanomaterials to the environment, particularly from water and wastewater treatment systems, and in the estimation of the effect of manufacture and use of nanomaterials on the environment.

SUBMITTER: Qiu Z

PROVIDER: S-EPMC3323979 | biostudies-literature | 2012 Mar

REPOSITORIES: biostudies-literature

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Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera.

Qiu Zhigang Z Yu Yunmei Y Chen Zhaoli Z Jin Min M Yang Dong D Zhao Zuguo Z Wang Jingfeng J Shen Zhiqiang Z Wang Xinwei X Qian Di D Huang Aihua A Zhang Buchang B Li Jun-Wen JW

Proceedings of the National Academy of Sciences of the United States of America 20120312 13

Antibiotic resistance is a worldwide public health concern. Conjugative transfer between closely related strains or species of bacteria is an important method for the horizontal transfer of multidrug-resistance genes. The extent to which nanomaterials are able to cause an increase in antibiotic resistance by the regulation of the conjugative transfer of antibiotic-resistance genes in bacteria, especially across genera, is still unknown. Here we show that nanomaterials in water can significantly ...[more]

PMID: 22411796

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Project description:By providing the bacterial cell with protection against several antibiotics at once, multiresistance plasmids have an evolutionary advantage in situations where antibiotic treatments are common, such as in hospital environments. However, resistance plasmids can also impose fitness costs on the bacterium in the absence of antibiotics, something that may limit their evolutionary success. The underlying mechanisms and the possible contribution of resistance genes to such costs are still largely not understood. Here, we have specifically investigated the contribution of plasmid-borne resistance genes to the reduced fitness of the bacterial cell. The pUUH239.2 plasmid carries 13 genes linked to antibiotic resistance and reduces bacterial fitness by 2.9% per generation. This cost is fully ameliorated by the removal of the resistance cassette. While most of the plasmid-borne resistance genes individually were cost-free, even when overexpressed, two specific gene clusters were responsible for the entire cost of the plasmid: the extended-spectrum-β-lactamase gene blaCTX-M-15 and the tetracycline resistance determinants tetAR. The blaCTX-M-15 cost was linked to the signal peptide that exports the β-lactamase into the periplasm, and replacement with an alternative signal peptide abolished the cost. Both the tetracycline pump TetA and its repressor TetR conferred a cost on the host cell, and the reciprocal expression of these genes is likely fine-tuned to balance the respective costs. These findings highlight that the cost of clinical multiresistance plasmids can be largely due to particular resistance genes and their interaction with other cellular systems, while other resistance genes and the plasmid backbone can be cost-free. IMPORTANCE Multiresistance plasmids are one of the main drivers of antibiotic resistance development and spread. Their evolutionary success through the accumulation and mobilization of resistance genes is central to resistance evolution. In this study, we find that the cost of the introduction of a multiresistance plasmid was completely attributable to resistance genes, while the rest of the plasmid backbone is cost-free. The majority of resistance genes on the plasmid had no appreciable cost to the host cell even when overexpressed, indicating that plasmid-borne resistance can be cost-free. In contrast, the widespread genes blaCTX-M-15 and tetAR were found to confer the whole cost of the plasmid by affecting specific cellular functions. These findings highlight how the evolution of resistance on plasmids is dependent on the amelioration of associated fitness costs and point at a conundrum regarding the high cost of some of the most widespread β-lactamase genes.

Dataset Information

Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera.

Publications

Nanoalumina promotes the horizontal transfer of multiresistance genes mediated by plasmids across genera.

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