Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.

Many studies have been devoted to understand the mechanisms used by pathogenic bacteria to exploit human hosts. These mechanisms are very diverse in the detail, but share commonalities whose quantification should enlighten the evolution of virulence from both a molecular and an ecological perspectiv...

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Autores principales: João Alves Gama, Sophie S Abby, Sara Vieira-Silva, Francisco Dionisio, Eduardo P C Rocha
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Publicado: Public Library of Science (PLoS) 2012
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Acceso en línea:https://doaj.org/article/e14d41a2b3f247d69675ee09e2030857
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spelling oai:doaj.org-article:e14d41a2b3f247d69675ee09e20308572021-11-18T06:04:49ZImmune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.1553-73661553-737410.1371/journal.ppat.1002503https://doaj.org/article/e14d41a2b3f247d69675ee09e20308572012-02-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22319444/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Many studies have been devoted to understand the mechanisms used by pathogenic bacteria to exploit human hosts. These mechanisms are very diverse in the detail, but share commonalities whose quantification should enlighten the evolution of virulence from both a molecular and an ecological perspective. We mined the literature for experimental data on infectious dose of bacterial pathogens in humans (ID50) and also for traits with which ID50 might be associated. These compilations were checked and complemented with genome analyses. We observed that ID50 varies in a continuous way by over 10 orders of magnitude. Low ID50 values are very strongly associated with the capacity of the bacteria to kill professional phagocytes or to survive in the intracellular milieu of these cells. Inversely, high ID50 values are associated with motile and fast-growing bacteria that use quorum-sensing based regulation of virulence factors expression. Infectious dose is not associated with genome size and shows insignificant phylogenetic inertia, in line with frequent virulence shifts associated with the horizontal gene transfer of a small number of virulence factors. Contrary to previous proposals, infectious dose shows little dependence on contact-dependent secretion systems and on the natural route of exposure. When all variables are combined, immune subversion and quorum-sensing are sufficient to explain two thirds of the variance in infectious dose. Our results show the key role of immune subversion in effective human infection by small bacterial populations. They also suggest that cooperative processes might be important for successful infection by bacteria with high ID50. Our results suggest that trade-offs between selection for population growth-related traits and selection for the ability to subvert the immune system shape bacterial infectiousness. Understanding these trade-offs provides guidelines to study the evolution of virulence and in particular the micro-evolutionary paths of emerging pathogens.João Alves GamaSophie S AbbySara Vieira-SilvaFrancisco DionisioEduardo P C RochaPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 8, Iss 2, p e1002503 (2012)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
João Alves Gama
Sophie S Abby
Sara Vieira-Silva
Francisco Dionisio
Eduardo P C Rocha
Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.
description Many studies have been devoted to understand the mechanisms used by pathogenic bacteria to exploit human hosts. These mechanisms are very diverse in the detail, but share commonalities whose quantification should enlighten the evolution of virulence from both a molecular and an ecological perspective. We mined the literature for experimental data on infectious dose of bacterial pathogens in humans (ID50) and also for traits with which ID50 might be associated. These compilations were checked and complemented with genome analyses. We observed that ID50 varies in a continuous way by over 10 orders of magnitude. Low ID50 values are very strongly associated with the capacity of the bacteria to kill professional phagocytes or to survive in the intracellular milieu of these cells. Inversely, high ID50 values are associated with motile and fast-growing bacteria that use quorum-sensing based regulation of virulence factors expression. Infectious dose is not associated with genome size and shows insignificant phylogenetic inertia, in line with frequent virulence shifts associated with the horizontal gene transfer of a small number of virulence factors. Contrary to previous proposals, infectious dose shows little dependence on contact-dependent secretion systems and on the natural route of exposure. When all variables are combined, immune subversion and quorum-sensing are sufficient to explain two thirds of the variance in infectious dose. Our results show the key role of immune subversion in effective human infection by small bacterial populations. They also suggest that cooperative processes might be important for successful infection by bacteria with high ID50. Our results suggest that trade-offs between selection for population growth-related traits and selection for the ability to subvert the immune system shape bacterial infectiousness. Understanding these trade-offs provides guidelines to study the evolution of virulence and in particular the micro-evolutionary paths of emerging pathogens.
format article
author João Alves Gama
Sophie S Abby
Sara Vieira-Silva
Francisco Dionisio
Eduardo P C Rocha
author_facet João Alves Gama
Sophie S Abby
Sara Vieira-Silva
Francisco Dionisio
Eduardo P C Rocha
author_sort João Alves Gama
title Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.
title_short Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.
title_full Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.
title_fullStr Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.
title_full_unstemmed Immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.
title_sort immune subversion and quorum-sensing shape the variation in infectious dose among bacterial pathogens.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/e14d41a2b3f247d69675ee09e2030857
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AT franciscodionisio immunesubversionandquorumsensingshapethevariationininfectiousdoseamongbacterialpathogens
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