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A diverse intrinsic antibiotic resistome from a cave bacterium

Andrew C. Pawlowski, Wenliang Wang, Kalinka Koteva, Hazel A. Barton, Andrew G. McArthur & Gerard D. Wright

Nature Communications 7, Article number: 13803 (2016)


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Antimicrobial resistanceBacterial evolutionEnzymes

Received: 05 July 2016 Accepted: 01 November 2016 Published online: 08 December 2016

Paenibacillus vortex colony - Eshel Ben Jacob

Abstract

Antibiotic resistance is ancient and widespread in environmental bacteria. These are therefore reservoirs of resistance elements and reflective of the natural history of antibiotics and resistance. In a previous study, we discovered that multi-drug resistance is common in bacteria isolated from Lechuguilla Cave, an underground ecosystem that has been isolated from the surface for over 4 Myr. Here we use whole-genome sequencing, functional genomics and biochemical assays to reveal the intrinsic resistome of Paenibacillus sp. LC231, a cave bacterial isolate that is resistant to most clinically used antibiotics. We systematically link resistance phenotype to genotype and in doing so, identify 18 chromosomal resistance elements, including five determinants without characterized homologues and three mechanisms not previously shown to be involved in antibiotic resistance. A resistome comparison across related surface Paenibacillus affirms the conservation of resistance over millions of years and establishes the longevity of these genes in this genus.

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How to cite this article: Pawlowski, A. C. et al. A diverse intrinsic antibiotic resistome from a cave bacterium. Nat. Commun. 7, 13803 doi: 10.1038/ncomms13803 (2016).

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Acknowledgements

We thank members of the CARD team for input into antibiotic resistance sequence analysis. We also thank Nicholas Waglechner (McMaster University) for helpful discussions in generating the Paenibacillus species tree and Christine King (McMaster University) for genome sequencing and shearing genomic DNA. This research was funded by a Canadian Institutes of Health Research Grant (MT-13536), Natural Sciences and Engineering Research Council Grant (237480) and by a Canada Research Chair in Antibiotic Biochemistry (to G.D.W). A.G.M. holds a Cisco Research Chair in Bioinformatics, supported by Cisco Systems Canada, Inc.

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Affiliations

Michael G. DeGroote Institute for Infectious Disease Research and the Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada L8S 4K1

Andrew C. Pawlowski, Wenliang Wang, Kalinka Koteva, Andrew G. McArthur & Gerard D. Wright

Department of Biology, University of Akron, Akron, Ohio 44325, USA

Hazel A. Barton

Contributions

A.C.P. performed all experiments except for structural elucidation using NMR. W.W. assisted in acetyl-capreomycin purification and performed acetyl-capreomycin NMR experiments. K.K. assisted in purifying descladinose clarithromycin and structural characterization of inactivated bacitracin, and performed descladinose clarithromycin NMR experiments. A.G.M. assisted the antibiotic resistance sequence analysis. H.A.B. collected strains and provided growth parameters. A.C.P and G.D.W. designed research and wrote the paper with contributions from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Gerard D. Wright.