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Bacterial Adaptation to Venom in Snakes and Arachnida

Animal venoms are considered sterile sources of antimicrobial compounds with strong membrane-disrupting activity against multidrug-resistant bacteria. However, venomous bite wound infections are common in developing nations. Investigating the envenomation organ and venom microbiota of five snake and...

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Autores principales: Esmaeilishirazifard, Elham, Usher, Louise, Trim, Carol, Denise, Hubert, Sangal, Vartul, Tyson, Gregory H., Barlow, Axel, Redway, Keith F., Taylor, John D., Kremyda-Vlachou, Myrto, Davies, Sam, Loftus, Teresa D., Lock, Mikaella M. G., Wright, Kstir, Dalby, Andrew, Snyder, Lori A. S., Wuster, Wolfgang, Trim, Steve, Moschos, Sterghios A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9248900/
https://www.ncbi.nlm.nih.gov/pubmed/35604233
http://dx.doi.org/10.1128/spectrum.02408-21
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author Esmaeilishirazifard, Elham
Usher, Louise
Trim, Carol
Denise, Hubert
Sangal, Vartul
Tyson, Gregory H.
Barlow, Axel
Redway, Keith F.
Taylor, John D.
Kremyda-Vlachou, Myrto
Davies, Sam
Loftus, Teresa D.
Lock, Mikaella M. G.
Wright, Kstir
Dalby, Andrew
Snyder, Lori A. S.
Wuster, Wolfgang
Trim, Steve
Moschos, Sterghios A.
author_facet Esmaeilishirazifard, Elham
Usher, Louise
Trim, Carol
Denise, Hubert
Sangal, Vartul
Tyson, Gregory H.
Barlow, Axel
Redway, Keith F.
Taylor, John D.
Kremyda-Vlachou, Myrto
Davies, Sam
Loftus, Teresa D.
Lock, Mikaella M. G.
Wright, Kstir
Dalby, Andrew
Snyder, Lori A. S.
Wuster, Wolfgang
Trim, Steve
Moschos, Sterghios A.
author_sort Esmaeilishirazifard, Elham
collection PubMed
description Animal venoms are considered sterile sources of antimicrobial compounds with strong membrane-disrupting activity against multidrug-resistant bacteria. However, venomous bite wound infections are common in developing nations. Investigating the envenomation organ and venom microbiota of five snake and two spider species, we observed venom community structures that depend on the host venomous animal species and evidenced recovery of viable microorganisms from black-necked spitting cobra (Naja nigricollis) and Indian ornamental tarantula (Poecilotheria regalis) venoms. Among the bacterial isolates recovered from N. nigricollis, we identified two venom-resistant, novel sequence types of Enterococcus faecalis whose genomes feature 16 virulence genes, indicating infectious potential, and 45 additional genes, nearly half of which improve bacterial 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. IMPORTANCE Notwithstanding their 3 to 5% mortality, the 2.7 million envenomation-related injuries occurring annually—predominantly across Africa, Asia, and Latin America—are also major causes of morbidity. Venom toxin-damaged tissue will develop infections in some 75% of envenomation victims, with E. faecalis being a common culprit of disease; however, such infections are generally considered to be independent of envenomation. Here, we provide evidence on venom microbiota across snakes and arachnida and report on the convergent evolution mechanisms that can facilitate adaptation to black-necked cobra venom in two independent E. faecalis strains, easily misidentified by biochemical diagnostics. Therefore, since inoculation with viable and virulence gene-harboring bacteria can occur during envenomation, acute infection risk management following envenomation is warranted, particularly for immunocompromised and malnourished victims in resource-limited settings. These results shed light on how bacteria evolve for survival in one of the most extreme environments on Earth and how venomous bites must be also treated for infections.
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spelling pubmed-92489002022-07-02 Bacterial Adaptation to Venom in Snakes and Arachnida Esmaeilishirazifard, Elham Usher, Louise Trim, Carol Denise, Hubert Sangal, Vartul Tyson, Gregory H. Barlow, Axel Redway, Keith F. Taylor, John D. Kremyda-Vlachou, Myrto Davies, Sam Loftus, Teresa D. Lock, Mikaella M. G. Wright, Kstir Dalby, Andrew Snyder, Lori A. S. Wuster, Wolfgang Trim, Steve Moschos, Sterghios A. Microbiol Spectr Research Article Animal venoms are considered sterile sources of antimicrobial compounds with strong membrane-disrupting activity against multidrug-resistant bacteria. However, venomous bite wound infections are common in developing nations. Investigating the envenomation organ and venom microbiota of five snake and two spider species, we observed venom community structures that depend on the host venomous animal species and evidenced recovery of viable microorganisms from black-necked spitting cobra (Naja nigricollis) and Indian ornamental tarantula (Poecilotheria regalis) venoms. Among the bacterial isolates recovered from N. nigricollis, we identified two venom-resistant, novel sequence types of Enterococcus faecalis whose genomes feature 16 virulence genes, indicating infectious potential, and 45 additional genes, nearly half of which improve bacterial 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. IMPORTANCE Notwithstanding their 3 to 5% mortality, the 2.7 million envenomation-related injuries occurring annually—predominantly across Africa, Asia, and Latin America—are also major causes of morbidity. Venom toxin-damaged tissue will develop infections in some 75% of envenomation victims, with E. faecalis being a common culprit of disease; however, such infections are generally considered to be independent of envenomation. Here, we provide evidence on venom microbiota across snakes and arachnida and report on the convergent evolution mechanisms that can facilitate adaptation to black-necked cobra venom in two independent E. faecalis strains, easily misidentified by biochemical diagnostics. Therefore, since inoculation with viable and virulence gene-harboring bacteria can occur during envenomation, acute infection risk management following envenomation is warranted, particularly for immunocompromised and malnourished victims in resource-limited settings. These results shed light on how bacteria evolve for survival in one of the most extreme environments on Earth and how venomous bites must be also treated for infections. American Society for Microbiology 2022-05-23 /pmc/articles/PMC9248900/ /pubmed/35604233 http://dx.doi.org/10.1128/spectrum.02408-21 Text en Copyright © 2022 Esmaeilishirazifard et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Esmaeilishirazifard, Elham
Usher, Louise
Trim, Carol
Denise, Hubert
Sangal, Vartul
Tyson, Gregory H.
Barlow, Axel
Redway, Keith F.
Taylor, John D.
Kremyda-Vlachou, Myrto
Davies, Sam
Loftus, Teresa D.
Lock, Mikaella M. G.
Wright, Kstir
Dalby, Andrew
Snyder, Lori A. S.
Wuster, Wolfgang
Trim, Steve
Moschos, Sterghios A.
Bacterial Adaptation to Venom in Snakes and Arachnida
title Bacterial Adaptation to Venom in Snakes and Arachnida
title_full Bacterial Adaptation to Venom in Snakes and Arachnida
title_fullStr Bacterial Adaptation to Venom in Snakes and Arachnida
title_full_unstemmed Bacterial Adaptation to Venom in Snakes and Arachnida
title_short Bacterial Adaptation to Venom in Snakes and Arachnida
title_sort bacterial adaptation to venom in snakes and arachnida
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9248900/
https://www.ncbi.nlm.nih.gov/pubmed/35604233
http://dx.doi.org/10.1128/spectrum.02408-21
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