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Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions

BACKGROUND: Infection processes consist of a sequence of steps, each critical for the interaction between host and parasite. Studies of host-parasite interactions rarely take into account the fact that different steps might be influenced by different factors and might, therefore, make different cont...

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Autores principales: Duneau, David, Luijckx, Pepijn, Ben-Ami, Frida, Laforsch, Christian, Ebert, Dieter
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3052238/
https://www.ncbi.nlm.nih.gov/pubmed/21342515
http://dx.doi.org/10.1186/1741-7007-9-11
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author Duneau, David
Luijckx, Pepijn
Ben-Ami, Frida
Laforsch, Christian
Ebert, Dieter
author_facet Duneau, David
Luijckx, Pepijn
Ben-Ami, Frida
Laforsch, Christian
Ebert, Dieter
author_sort Duneau, David
collection PubMed
description BACKGROUND: Infection processes consist of a sequence of steps, each critical for the interaction between host and parasite. Studies of host-parasite interactions rarely take into account the fact that different steps might be influenced by different factors and might, therefore, make different contributions to shaping coevolution. We designed a new method using the Daphnia magna - Pasteuria ramosa system, one of the rare examples where coevolution has been documented, in order to resolve the steps of the infection and analyse the factors that influence each of them. RESULTS: Using the transparent Daphnia hosts and fluorescently-labelled spores of the bacterium P. ramosa, we identified a sequence of infection steps: encounter between parasite and host; activation of parasite dormant spores; attachment of spores to the host; and parasite proliferation inside the host. The chances of encounter had been shown to depend on host genotype and environment. We tested the role of genetic and environmental factors in the newly described activation and attachment steps. Hosts of different genotypes, gender and species were all able to activate endospores of all parasite clones tested in different environments; suggesting that the activation cue is phylogenetically conserved. We next established that parasite attachment occurs onto the host oesophagus independently of host species, gender and environmental conditions. In contrast to spore activation, attachment depended strongly on the combination of host and parasite genotypes. CONCLUSIONS: Our results show that different steps are influenced by different factors. Host-type-independent spore activation suggests that this step can be ruled out as a major factor in Daphnia-Pasteuria coevolution. On the other hand, we show that the attachment step is crucial for the pronounced genetic specificities of this system. We suggest that this one step can explain host population structure and could be a key force behind coevolutionary cycles. We discuss how different steps can explain different aspects of the coevolutionary dynamics of the system: the properties of the attachment step, explaining the rapid evolution of infectivity and the properties of later parasite proliferation explaining the evolution of virulence. Our study underlines the importance of resolving the infection process in order to better understand host-parasite interactions.
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spelling pubmed-30522382011-03-10 Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions Duneau, David Luijckx, Pepijn Ben-Ami, Frida Laforsch, Christian Ebert, Dieter BMC Biol Research Article BACKGROUND: Infection processes consist of a sequence of steps, each critical for the interaction between host and parasite. Studies of host-parasite interactions rarely take into account the fact that different steps might be influenced by different factors and might, therefore, make different contributions to shaping coevolution. We designed a new method using the Daphnia magna - Pasteuria ramosa system, one of the rare examples where coevolution has been documented, in order to resolve the steps of the infection and analyse the factors that influence each of them. RESULTS: Using the transparent Daphnia hosts and fluorescently-labelled spores of the bacterium P. ramosa, we identified a sequence of infection steps: encounter between parasite and host; activation of parasite dormant spores; attachment of spores to the host; and parasite proliferation inside the host. The chances of encounter had been shown to depend on host genotype and environment. We tested the role of genetic and environmental factors in the newly described activation and attachment steps. Hosts of different genotypes, gender and species were all able to activate endospores of all parasite clones tested in different environments; suggesting that the activation cue is phylogenetically conserved. We next established that parasite attachment occurs onto the host oesophagus independently of host species, gender and environmental conditions. In contrast to spore activation, attachment depended strongly on the combination of host and parasite genotypes. CONCLUSIONS: Our results show that different steps are influenced by different factors. Host-type-independent spore activation suggests that this step can be ruled out as a major factor in Daphnia-Pasteuria coevolution. On the other hand, we show that the attachment step is crucial for the pronounced genetic specificities of this system. We suggest that this one step can explain host population structure and could be a key force behind coevolutionary cycles. We discuss how different steps can explain different aspects of the coevolutionary dynamics of the system: the properties of the attachment step, explaining the rapid evolution of infectivity and the properties of later parasite proliferation explaining the evolution of virulence. Our study underlines the importance of resolving the infection process in order to better understand host-parasite interactions. BioMed Central 2011-02-22 /pmc/articles/PMC3052238/ /pubmed/21342515 http://dx.doi.org/10.1186/1741-7007-9-11 Text en Copyright ©2011 Duneau et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Duneau, David
Luijckx, Pepijn
Ben-Ami, Frida
Laforsch, Christian
Ebert, Dieter
Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
title Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
title_full Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
title_fullStr Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
title_full_unstemmed Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
title_short Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
title_sort resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3052238/
https://www.ncbi.nlm.nih.gov/pubmed/21342515
http://dx.doi.org/10.1186/1741-7007-9-11
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