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Microbial adaptation to venom is common in snakes and spiders

E. Esmaeilishirazifard, L. Usher, C. Trim, H. Denise, V. Sangal, G.H. Tyson, A. Barlow, K.F. Redway, J.D. Taylor, M. Kremyda-Vlachou, S. Davies, T. D. Loftus, M.M.G. Lock, K. Wright, A. Dalby, L.A.S. Snyder, W. Wuster, S. Trim, View ORCID ProfileS.A. Moschos
doi: https://doi.org/10.1101/348433
E. Esmaeilishirazifard
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
2Westminster Genomic Services, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
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L. Usher
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
2Westminster Genomic Services, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
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C. Trim
3School of Psychology and Life Sciences, Faculty of Science, Engineering and Social Sciences, Canterbury Christ Church University, Canterbury, Kent, U.K.
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H. Denise
4EMBL-EBI European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK
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V. Sangal
5Department of Applied Sciences, Faculty of Health and Life Sciences, Northumbria University, Newcastle, Tyne and Wear, UK
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G.H. Tyson
6Food and Drug Administration, Center for Veterinary Medicine, Office of Research. Laurel, MD, USA
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A. Barlow
7Institute for Biochemistry and Biology, University of Potsdam, Potsdam, Germany
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K.F. Redway
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
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J.D. Taylor
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
2Westminster Genomic Services, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
8School of Environment and Life Sciences, University of Salford, Salford, Greater Manchester, U.K.
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M. Kremyda-Vlachou
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
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S. Davies
5Department of Applied Sciences, Faculty of Health and Life Sciences, Northumbria University, Newcastle, Tyne and Wear, UK
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T. D. Loftus
9Venomtech Limited, Discovery Park, Sandwich, Kent, UK
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M.M.G. Lock
9Venomtech Limited, Discovery Park, Sandwich, Kent, UK
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K. Wright
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
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A. Dalby
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
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L.A.S. Snyder
10School of Life Sciences, Pharmacy, and Chemistry, Kingston University, Kingston Upon Thames, London, UK
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W. Wuster
11School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, Wales, U.K.
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S. Trim
9Venomtech Limited, Discovery Park, Sandwich, Kent, UK
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S.A. Moschos
1Department of Biomedical Sciences, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
2Westminster Genomic Services, Faculty of Science and Technology, University of Westminster, London, U.K., E.U.
5Department of Applied Sciences, Faculty of Health and Life Sciences, Northumbria University, Newcastle, Tyne and Wear, UK
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  • ORCID record for S.A. Moschos
  • For correspondence: sterghios.moschos@northumbria.ac.uk
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Abstract

Animal venoms are considered sterile sources of antimicrobial compounds with strong membrane disrupting activity against multi-drug resistant bacteria. However, bite wound infections are common in developing nations. Investigating the oral and venom microbiome of five snake and two spider species, we evidence viable microorganisms potentially unique to venom for black-necked spitting cobras (Naja nigricollis). Among these are two venom-resistant novel sequence types of Enterococcus faecalis; the genome sequence data of these isolates feature an additional 45 genes, nearly half of which improve membrane integrity. Our findings challenge the dogma of venom sterility and indicate an increased primary infection risk in the clinical management of venomous animal bite wounds.

One Sentence Summary Independent bacterial colonization of cobra venom drives acquisition of genes antagonistic to venom antimicrobial peptides.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • We have added significant new data in our manuscript consisting of 1) MIC curves of the venom-derived E. faecalis isolates vs V583 demonstrating venom tolerance and 2) expanding pangenomic comparisons to 723 additional published E. faecalis genomes, in an attempt to identify the source of the venom-tolerant isolates. These isolates show no, or >30% inhibition by venom at 50mg/ml, where V583 shows an MIC of 11.7 mg/ml and an NIC 2.78 mg/ml. In addition, we redefine the pangenome of E. faecalis at 26,412 genes with a core genome of 342 highly conserved genes and 865 genes present in over 99% of strains. Maximum likelihood trees also failed to place the venom-derived strains within clades identified from within the UK or with any environmental or other link to the source snakes demonstrating independent adaptation to the venom milieu.

Copyright 
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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Microbial adaptation to venom is common in snakes and spiders
E. Esmaeilishirazifard, L. Usher, C. Trim, H. Denise, V. Sangal, G.H. Tyson, A. Barlow, K.F. Redway, J.D. Taylor, M. Kremyda-Vlachou, S. Davies, T. D. Loftus, M.M.G. Lock, K. Wright, A. Dalby, L.A.S. Snyder, W. Wuster, S. Trim, S.A. Moschos
bioRxiv 348433; doi: https://doi.org/10.1101/348433
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Microbial adaptation to venom is common in snakes and spiders
E. Esmaeilishirazifard, L. Usher, C. Trim, H. Denise, V. Sangal, G.H. Tyson, A. Barlow, K.F. Redway, J.D. Taylor, M. Kremyda-Vlachou, S. Davies, T. D. Loftus, M.M.G. Lock, K. Wright, A. Dalby, L.A.S. Snyder, W. Wuster, S. Trim, S.A. Moschos
bioRxiv 348433; doi: https://doi.org/10.1101/348433

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