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The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence

Pramod K. Jangir, Lois Ogunlana, Petra Szili, Márton Czikkely, Emily J. Stevens, Yu Yang, Qiue Yang, Yang Wang, Csaba Pál, Timothy R. Walsh, Craig MacLean
doi: https://doi.org/10.1101/2022.02.12.480185
Pramod K. Jangir
1Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK
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  • For correspondence: jangirk.pramod@gmail.com pramod.jangir@zoo.ox.ac.uk craig.maclean@zoo.ox.ac.uk
Lois Ogunlana
1Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK
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Petra Szili
2Synthetic and Systems Biology Unit, Biological Research Centre, Eötvös Loránd Research Network (ELKH), Szeged, Hungary
3Doctoral School of Multidisciplinary Medical Sciences, University of Szeged, Szeged, Hungary
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Márton Czikkely
2Synthetic and Systems Biology Unit, Biological Research Centre, Eötvös Loránd Research Network (ELKH), Szeged, Hungary
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Emily J. Stevens
1Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK
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Yu Yang
4Guangdong Provincial Key Laboratory of Veterinary Pharmaceutics Development and Safety Evaluation, South China Agricultural University, Guangzhou, China
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Qiue Yang
5Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China
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Yang Wang
6Beijing Advanced Innovation Centre for Food Nutrition and Human Health, College of Veterinary Medicine, China Agricultural University, Beijing, 100193, China
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Csaba Pál
2Synthetic and Systems Biology Unit, Biological Research Centre, Eötvös Loránd Research Network (ELKH), Szeged, Hungary
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Timothy R. Walsh
1Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK
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Craig MacLean
1Department of Zoology, University of Oxford, Oxford, OX1 3PS, UK
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  • For correspondence: jangirk.pramod@gmail.com pramod.jangir@zoo.ox.ac.uk craig.maclean@zoo.ox.ac.uk
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Abstract

Antimicrobial peptides (AMPs) offer a promising solution to the antibiotic resistance crisis. However, an unresolved serious concern is that the evolution of resistance to therapeutic AMPs may generate cross-resistance to host AMPs, compromising a cornerstone of the innate immune response. We systematically tested this hypothesis using globally disseminated mobile colistin resistance (MCR) that has been selected by the use of colistin in agriculture and medicine. Here we show that MCR provides a selective advantage to E. coli in the presence of key AMPs from humans and agricultural animals by increasing AMP resistance. Moreover, MCR promotes bacterial growth in human serum and increases virulence in a Galleria mellonella infection model. Our study shows how the anthropogenic use of AMPs can drive the accidental evolution of resistance to the innate immune system of humans and animals. These findings have major implications for the design and use of therapeutic AMPs and they suggest that MCR will be difficult to eradicate, even if colistin use is withdrawn.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 12, 2022.
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The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
Pramod K. Jangir, Lois Ogunlana, Petra Szili, Márton Czikkely, Emily J. Stevens, Yu Yang, Qiue Yang, Yang Wang, Csaba Pál, Timothy R. Walsh, Craig MacLean
bioRxiv 2022.02.12.480185; doi: https://doi.org/10.1101/2022.02.12.480185
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The evolution of colistin resistance increases bacterial resistance to host antimicrobial peptides and virulence
Pramod K. Jangir, Lois Ogunlana, Petra Szili, Márton Czikkely, Emily J. Stevens, Yu Yang, Qiue Yang, Yang Wang, Csaba Pál, Timothy R. Walsh, Craig MacLean
bioRxiv 2022.02.12.480185; doi: https://doi.org/10.1101/2022.02.12.480185

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