Cargando…
Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model
Infectious endocarditis (IE) is an uncommon disease with significant morbidity and mortality. The pathogenesis of IE has historically been described as a cascade of host-specific events beginning with endothelial damage and thrombus formation and followed by bacterial colonization of the nascent thr...
Autores principales: | , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557322/ https://www.ncbi.nlm.nih.gov/pubmed/34734186 http://dx.doi.org/10.1093/femsmc/xtab014 |
_version_ | 1784592351112462336 |
---|---|
author | Barnes, Aaron M T Frank, Kristi L Dale, Jennifer L Manias, Dawn A Powers, Jennifer L Dunny, Gary M |
author_facet | Barnes, Aaron M T Frank, Kristi L Dale, Jennifer L Manias, Dawn A Powers, Jennifer L Dunny, Gary M |
author_sort | Barnes, Aaron M T |
collection | PubMed |
description | Infectious endocarditis (IE) is an uncommon disease with significant morbidity and mortality. The pathogenesis of IE has historically been described as a cascade of host-specific events beginning with endothelial damage and thrombus formation and followed by bacterial colonization of the nascent thrombus. Enterococcus faecalis is a Gram-positive commensal bacterial member of the gastrointestinal tract microbiota in most terrestrial animals and a leading cause of opportunistic biofilm-associated infections, including endocarditis. Here, we provide evidence that E. faecalis can colonize the endocardial surface without pre-existing damage and in the absence of thrombus formation in a rabbit endovascular infection model. Using previously described light and scanning electron microscopy techniques, we show that inoculation of a well-characterized E. faecalis lab strain in the marginal ear vein of New Zealand White rabbits resulted in rapid colonization of the endocardium throughout the heart within 4 days of administration. Unexpectedly, ultrastructural imaging revealed that the microcolonies were firmly attached directly to the endocardium in areas without morphological evidence of gross tissue damage. Further, the attached bacterial aggregates were not associated with significant cellular components of coagulation or host extracellular matrix damage repair (i.e. platelets). These results suggest that the canonical model of mechanical surface damage as a prerequisite for bacterial attachment to host sub-endothelial components is not required. Furthermore, these findings are consistent with a model of initial establishment of stable, endocarditis-associated E. faecalis biofilm microcolonies that may provide a reservoir for the eventual valvular infection characteristic of clinical endocarditis. The similarities between the E. faecalis colonization and biofilm morphologies seen in this rabbit endovascular infection model and our previously published murine gastrointestinal colonization model indicate that biofilm production and common host cell attachment factors are conserved in disparate mammalian hosts under both commensal and pathogenic contexts. |
format | Online Article Text |
id | pubmed-8557322 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-85573222021-11-01 Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model Barnes, Aaron M T Frank, Kristi L Dale, Jennifer L Manias, Dawn A Powers, Jennifer L Dunny, Gary M FEMS Microbes Research Article Infectious endocarditis (IE) is an uncommon disease with significant morbidity and mortality. The pathogenesis of IE has historically been described as a cascade of host-specific events beginning with endothelial damage and thrombus formation and followed by bacterial colonization of the nascent thrombus. Enterococcus faecalis is a Gram-positive commensal bacterial member of the gastrointestinal tract microbiota in most terrestrial animals and a leading cause of opportunistic biofilm-associated infections, including endocarditis. Here, we provide evidence that E. faecalis can colonize the endocardial surface without pre-existing damage and in the absence of thrombus formation in a rabbit endovascular infection model. Using previously described light and scanning electron microscopy techniques, we show that inoculation of a well-characterized E. faecalis lab strain in the marginal ear vein of New Zealand White rabbits resulted in rapid colonization of the endocardium throughout the heart within 4 days of administration. Unexpectedly, ultrastructural imaging revealed that the microcolonies were firmly attached directly to the endocardium in areas without morphological evidence of gross tissue damage. Further, the attached bacterial aggregates were not associated with significant cellular components of coagulation or host extracellular matrix damage repair (i.e. platelets). These results suggest that the canonical model of mechanical surface damage as a prerequisite for bacterial attachment to host sub-endothelial components is not required. Furthermore, these findings are consistent with a model of initial establishment of stable, endocarditis-associated E. faecalis biofilm microcolonies that may provide a reservoir for the eventual valvular infection characteristic of clinical endocarditis. The similarities between the E. faecalis colonization and biofilm morphologies seen in this rabbit endovascular infection model and our previously published murine gastrointestinal colonization model indicate that biofilm production and common host cell attachment factors are conserved in disparate mammalian hosts under both commensal and pathogenic contexts. Oxford University Press 2021-09-25 /pmc/articles/PMC8557322/ /pubmed/34734186 http://dx.doi.org/10.1093/femsmc/xtab014 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of FEMS. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
spellingShingle | Research Article Barnes, Aaron M T Frank, Kristi L Dale, Jennifer L Manias, Dawn A Powers, Jennifer L Dunny, Gary M Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model |
title |
Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model |
title_full |
Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model |
title_fullStr |
Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model |
title_full_unstemmed |
Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model |
title_short |
Enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model |
title_sort | enterococcus faecalis colonizes and forms persistent biofilm microcolonies on undamaged endothelial surfaces in a rabbit endovascular infection model |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8557322/ https://www.ncbi.nlm.nih.gov/pubmed/34734186 http://dx.doi.org/10.1093/femsmc/xtab014 |
work_keys_str_mv | AT barnesaaronmt enterococcusfaecaliscolonizesandformspersistentbiofilmmicrocoloniesonundamagedendothelialsurfacesinarabbitendovascularinfectionmodel AT frankkristil enterococcusfaecaliscolonizesandformspersistentbiofilmmicrocoloniesonundamagedendothelialsurfacesinarabbitendovascularinfectionmodel AT dalejenniferl enterococcusfaecaliscolonizesandformspersistentbiofilmmicrocoloniesonundamagedendothelialsurfacesinarabbitendovascularinfectionmodel AT maniasdawna enterococcusfaecaliscolonizesandformspersistentbiofilmmicrocoloniesonundamagedendothelialsurfacesinarabbitendovascularinfectionmodel AT powersjenniferl enterococcusfaecaliscolonizesandformspersistentbiofilmmicrocoloniesonundamagedendothelialsurfacesinarabbitendovascularinfectionmodel AT dunnygarym enterococcusfaecaliscolonizesandformspersistentbiofilmmicrocoloniesonundamagedendothelialsurfacesinarabbitendovascularinfectionmodel |