Bacterial Adaptation to Venom in Snakes and Arachnida

Esmaeilishirazifard, Elham, Usher, Louise, Trim, Carol, Denise, Hubert, Sangal, V., Tyson, G., 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, L., Wuster, Wolfgang, Trim, Steve and Moschos, S. 2022. Bacterial Adaptation to Venom in Snakes and Arachnida. Microbiology Spectrum. 10 (3) e02408-21. https://doi.org/10.1128/spectrum.02408-21

TitleBacterial Adaptation to Venom in Snakes and Arachnida
TypeJournal article
AuthorsEsmaeilishirazifard, Elham, Usher, Louise, Trim, Carol, Denise, Hubert, Sangal, V., Tyson, G., 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, L., Wuster, Wolfgang, Trim, Steve and Moschos, S.
AbstractAnimal 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 , 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. 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.
Keywordsmultidrug resistance
microbiome
venom
drug resistance evolution
extremophiles
genome analysis
Article numbere02408-21
JournalMicrobiology Spectrum
Journal citation10 (3)
ISSN2165-0497
Year2022
PublisherAmerican Society for Microbiology
Publisher's version
License
CC BY 4.0
File Access Level
Open (open metadata and files)
Digital Object Identifier (DOI)https://doi.org/10.1128/spectrum.02408-21
PubMed ID35604233
Publication dates
Published online23 May 2022

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Moschos, S.A., Bramwell, V.W. and Alpar, H.O. 2003. Considerations in the antigen-stimulated, primed, primary splenocyte culture model as an in vitro vaccine screening tool. Proceedings of the 30th International Symposium for the Controlled Release of Bioactive Materials. Glasgow 19 - 23 Jul 2003 pp. 899

The structure of human liver fructose-1,6-bisphosphate aldolase
Dalby, A.R., Tolan, D.R. and Littlechild, J.A. 2002. The structure of human liver fructose-1,6-bisphosphate aldolase. Acta Crystallographica Section D. D57, pp. 1526-1533. https://doi.org/10.1107/s0907444901012719

Structural and functional comparisons between vanadium haloperoxidase and acid phosphatase enzymes.
Littlechild, J., Garcia-Rodriguez, E., Dalby, A.R. and Isupov, M. 2002. Structural and functional comparisons between vanadium haloperoxidase and acid phosphatase enzymes. Journal of Molecular Recognition. 15 (5), pp. 291-296. https://doi.org/10.1002/jmr.590

Immunogenicity of adjuvanted recombinant urease administered intranasally
Moschos, S.A., Somavarapu, S., Singh, J., Bramwell, V.W., Randall, L., Guy, B. and Alpar, H.O. 2001. Immunogenicity of adjuvanted recombinant urease administered intranasally. Proceedings of the 28th International Symposium for the Controlled Release of Bioactive Materials. San Diego, USA 23 - 27 Jun 2001 pp. 7033

Immunogenicity of adjuvanted recombinant urease administered intra-muscularly
Moschos, S.A., Somavarapu, S., Eyles, J.E., McHugh, C., Bramwell, V.W., Randall, L., Guy, B. and Alpar, H.O. 2001. Immunogenicity of adjuvanted recombinant urease administered intra-muscularly. Proceedings of the 28th International Symposium for the Controlled Release of Bioactive Materials. San Diego, USA 23 - 27 Jun 2001 pp. 7033

Evaluation of adjuvanted recombinant urease for effective immunization against Helicobacter pylori
Moschos, S.A., Somavarapu, S., Eyles, J.E., McHugh, C., Bramwell, V.W., Randall, L., Guy, B. and Alpar, H.O. 2001. Evaluation of adjuvanted recombinant urease for effective immunization against Helicobacter pylori. Immunology. 104 (s1), p. 98. https://doi.org/10.1046/j.1365-2567.2001.1040s1070.x

Quil-A and MDP enhances the adjuvanticity of alum for intramuscular delivery of rURE
Moschos, S.A., Somavarapu, S., Bramwell, V.W., Randall, L., Guy, B. and Alpar, H.O. 2001. Quil-A and MDP enhances the adjuvanticity of alum for intramuscular delivery of rURE. Immunology. 104 (s1), p. 98. https://doi.org/10.1046/j.1365-2567.2001.1040s1070.x

Crystal structure of dodecameric vanadium-dependent bromoperoxidase from the red algae Corallina officinalis.
Isupov, M.N., Dalby, A.R., Brindley, A.A., Izumi, Y., Tanabe, T., Murshudov, G.N. and Littlechild, J.A. 2000. Crystal structure of dodecameric vanadium-dependent bromoperoxidase from the red algae Corallina officinalis. Journal of Molecular Biology. 299 (4), pp. 1035-1049. https://doi.org/10.1006/jmbi.2000.3806

Microsphere encapsulated Diphtheria Toxoid induces protein secretion from in-vitro Peyers’ patches and in vivo
Turner, J.J., Somavarapu, S., Moschos, S.A., Randall, L., Simpkin, G. and Alpar, H.O. 2000. Microsphere encapsulated Diphtheria Toxoid induces protein secretion from in-vitro Peyers’ patches and in vivo. Proceedings of the 3rd World Meeting APV/APGI 2000. Berlin, Germany 3 - 6 Apr 2000 pp. 389-390

Novel protein secretion from both ex-vivo Peyers’ patches and in-vivo; induction by microsphere encapsulated diphtheria toxoid
Moschos, S.A., Somavarapu, S., Singh, J., Bramwell, V.W., Randall, L., Guy, B. and Alpar, H.O. 2000. Novel protein secretion from both ex-vivo Peyers’ patches and in-vivo; induction by microsphere encapsulated diphtheria toxoid. Proceedings of the 27th International Symposium for the Controlled Release of Bioactive Materials. Paris, France 09 - 13 Jul 2001 pp. 562-563

Crystal structure of human muscle aldolase complexed with fructose 1,6-bisphosphate: mechanistic implications.
Dalby, A.R., Dauter, Z. and Littlechild, J.A. 1999. Crystal structure of human muscle aldolase complexed with fructose 1,6-bisphosphate: mechanistic implications. Protein Science. 8 (2), pp. 291-297. https://doi.org/10.1110/ps.8.2.291

Structure of a phosphoglycerate mutase:3-phosphoglyceric acid complex at 1.7 A.
Crowhurst, G.S., Dalby, A.R., Isupov, M.N., Campbell, J.W. and Littlechild, J.A. 1999. Structure of a phosphoglycerate mutase:3-phosphoglyceric acid complex at 1.7 A. Acta Crystallographica Section D. D55, pp. 1822-1826. https://doi.org/10.1107/s0907444999009944

Preliminary X-ray analysis of a new crystal form of the vanadium-dependent bromoperoxidase from Corallina officinalis.
Brindley, A.A., Dalby, A.R., Isupov, M.N. and Littlechild, J.A. 1998. Preliminary X-ray analysis of a new crystal form of the vanadium-dependent bromoperoxidase from Corallina officinalis. Acta Crystallographica Section D: Structural Biology. D54 (Pt 3), pp. 454-457. https://doi.org/10.1107/s0907444997014558

Studies with type I aldolase to understand fructose intolerance and combat parasitic disease.
Dalby, A.R. and Littlechild, J.A. 1996. Studies with type I aldolase to understand fructose intolerance and combat parasitic disease. Journal of Pharmacy and Pharmacology. 48 (2), pp. 214-217. https://doi.org/10.1111/j.2042-7158.1996.tb07126.x

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