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What Is a Pathogen? Toward a Process View of Host-Parasite Interactions Pierre-Olivier Methot, Samuel Alizon

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What Is a Pathogen? Toward a Process View of Host-Parasite Interactions Pierre-Olivier Methot, Samuel Alizon What is a pathogen? Toward a process view of host-parasite interactions Pierre-Olivier Methot, Samuel Alizon To cite this version: Pierre-Olivier Methot, Samuel Alizon. What is a pathogen? Toward a process view of host-parasite interactions. Virulence, Landes Bioscience, 2014, 5 (8), pp.775-85. 10.4161/21505594.2014.960726. hal-01567912 HAL Id: hal-01567912 https://hal.archives-ouvertes.fr/hal-01567912 Submitted on 5 May 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. This article was downloaded by: [82.237.92.107] On: 20 January 2015, At: 12:44 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Virulence Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/kvir20 What is a pathogen? Toward a process view of host- parasite interactions Pierre-Olivier Méthotab & Samuel Alizonc a Université Laval; Québec, Canada b Centre Interuniversitaire de Recherche sur la Science et la Technologie; Montréal, Canada c Laboratoire MIVEGEC (UMR CNRS-IRD-UM1-UM2 5290), Montpellier, France Accepted author version posted online: 29 Oct 2014.Published online: 20 Jan 2015. Click for updates To cite this article: Pierre-Olivier Méthot & Samuel Alizon (2014) What is a pathogen? Toward a process view of host-parasite interactions, Virulence, 5:8, 775-785, DOI: 10.4161/21505594.2014.960726 To link to this article: http://dx.doi.org/10.4161/21505594.2014.960726 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Versions of published Taylor & Francis and Routledge Open articles and Taylor & Francis and Routledge Open Select articles posted to institutional or subject repositories or any other third-party website are without warranty from Taylor & Francis of any kind, either expressed or implied, including, but not limited to, warranties of merchantability, fitness for a particular purpose, or non-infringement. Any opinions and views expressed in this article are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor & Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions It is essential that you check the license status of any given Open and Open Select article to confirm conditions of access and use. REVIEW Virulence 5:8, 775--785; November/December 2014; Published with license by Taylor & Francis Group, LLC What is a pathogen? Toward a process view of host-parasite interactions Pierre-Olivier Methot 1,2,* and Samuel Alizon3 1Universite Laval; Quebec, Canada; 2Centre Interuniversitaire de Recherche sur la Science et la Technologie; Montreal, Canada; 3Laboratoire MIVEGEC (UMR CNRS-IRD-UM1-UM2 5290), Montpellier, France Keywords: ecology, evolution, disease, infection, process, virulence th Until quite recently and since the late 19 century, 4 medical microbiology has been based on the assumption that body that can be disrupted. By 1850 in Europe, the ontological some micro-organisms are pathogens and others are not. This view, long associated with early theories of contagion, was largely binary view is now strongly criticized and is even becoming out of fashion. However, it did gain a new foothold with the rise of th untenable. We first provide a historical overview of the medical microbiology in the last quarter of the 19 century, and th 5 changing nature of host-parasite interactions, in which we enjoyed a lasting influence in the 20 century. argue that large-scale sequencing not only shows that More than mere historical curiosities, these models are reflected, identifying the roots of pathogenesis is much more at least partly, in current scientific concepts. The notion of a complicated than previously thought, but also forces us to ‘pathogen’, for example, was long understood along the lines of the reconsider what a pathogen is. To address the challenge of ontological model. A pathogen was seen as an essentially static or fi de ning a pathogen in post-genomic science, we present and unchanging entity, which was absolutely distinct from other types of discuss recent results that embrace the microbial genetic microbes in that it was believed to possess an inherent capacity to diversity (both within- and between-host) and underline the relevance of microbial ecology and evolution. By analyzing cause disease in hosts. The German bacteriologist Robert Koch, for instance, promoted a separation between ‘harmful’ microorganisms and extending earlier work on the concept of pathogen, we 6 th propose pathogenicity (or virulence) should be viewed as a and other ‘kinds’ of microbes. In the first decades of the 20 cen- dynamical feature of an interaction between a host and tury, American microbiologist Hans Zinsser divided microorgan- microbes. isms into ‘pure saprophytes’ (unable to grow in living tissues), ‘pure parasites’ (able to rapidly enter and reproduce in a healthy host), and ‘half parasites’ (low and context-sensitive invasive power).7 Anum- A century ago, Gertrude Stein told us that a rose is a rose is a rose, ber of medical bacteriologists in the 1950s, microbiologist Stanley but today, modern genomics is telling us that a pathogen is not a Falkow remembers, also ‘focused on differentiating the “good guys” 1 pathogen — Eric C. Keen from the “bad guys,” and a pathogen was simply defined as any organism that caused disease’.8 Even nowadays ‘most authorities Introduction divide microbes into those that are pathogenic and non-pathogenic’, according to immunologist and bacteriologist Arturo Casadevall.9 Downloaded by [82.237.92.107] at 12:44 20 January 2015 Medical historians describe how diseases were seen either as Butwhatifapathogenisnotalwaysapathogen? ‘things’ or ‘processes’, and how this led to what are now known as By analyzing several significant conceptual shifts in our ways of the ‘ontological’ and the ‘physiological’ models of disease.2 Accord- thinking about microorganisms and their hosts, we show how scien- ing to the ontological model, a disease is a foreign entity (either ani- tists are now embracing a version of the physiological, process-ori- mate or inert), or an object ‘lodged in the body’.3 Ultimately, curing ented model of host-parasite interactions. Here, our use of the term disease and restoring health amounts to expelling the intruder. In parasite is ecological (see the Glossary) and includes both micro- contrast, the physiological model frames a disease as a disturbance or parasites (e.g., viruses and bacteria) and macro-parasites (e.g., as a deviation from the norm, and includes a temporal aspect. In this worms), and we define the concept of host-parasite relation as an dynamic conceptualisation, health corresponds to the harmony or interactive biological system, whose outcome is indeterminate and equilibrium established between the elementary qualities of the depends largely on the ecological context it inhabits. Our main thesis is that a better understanding of virulence (i.e., © Pierre-Olivier Methot and Samuel Alizon the decrease in host fitness due to the infection) could be achieved if *Correspondence to: Pierre-Olivier Methot; Email: p.olivier.methot@gmail we asked under what (ecological) circumstances a microorganism .com acquires the capacity to bring about disease in a host, rather than Submitted: 01/31/2014; Revised: 07/12/2014; Accepted: 08/27/2014 http://dx.doi.org/10.4161/21505594.2014.960726 looking for some specific attributes that might demarcate pathogens This is an Open Access article distributed under the terms of the Creative from commensals. In fact, the boundaries between commensalism, Commons Attribution-Non-Commercial License (http://creativecommons. parasitism and mutualism are fluid, and these interactions may best org/licenses/by-nc/3.0/), which permits unrestricted non-commercial use, be viewed as a continuum rather than as fixed categories in nature distribution, and reproduction in any medium, provided the original work is (Fig. 1). Indeed, ‘symbiotic associations’ can easily go from one to properly cited. The moral rights of the named author(s) have been asserted. the other following small ecological changes.10 www.landesbioscience.com Virulence 775 Fig. 1. Spatial
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