High Virulence of Wolbachia after Host Switching: When Autophagy Hurts
Publication Date
August 02, 2012
Journal
PLOS Pathogens
Authors
Winka Le Clec'h, Christine Braquart Varnier, Maryline Raimond, Jean Baptiste Ferdy, et al
Volume
8
Issue
8
Pages
e1002844
DOI
https://dx.plos.org/10.1371/journal.ppat.1002844
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1002844
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/22876183
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3410869
Europe PMC
http://europepmc.org/abstract/MED/22876183
Web of Science
000308558000022
Scopus
84866165048
Mendeley
http://www.mendeley.com/research/high-virulence-wolbachia-after-host-switching-autophagy-hurts
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Mendeley | Further Information

{"title"=>"High Virulence of Wolbachia after Host Switching: When Autophagy Hurts", "type"=>"journal", "authors"=>[{"first_name"=>"Winka", "last_name"=>"Le Clec'h", "scopus_author_id"=>"55357555600"}, {"first_name"=>"Christine", "last_name"=>"Braquart-Varnier", "scopus_author_id"=>"8846889700"}, {"first_name"=>"Maryline", "last_name"=>"Raimond", "scopus_author_id"=>"23493712400"}, {"first_name"=>"Jean Baptiste", "last_name"=>"Ferdy", "scopus_author_id"=>"6602504405"}, {"first_name"=>"Didier", "last_name"=>"Bouchon", "scopus_author_id"=>"6701400506"}, {"first_name"=>"Mathieu", "last_name"=>"Sicard", "scopus_author_id"=>"56277710900"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-84866165048", "pui"=>"365631421", "doi"=>"10.1371/journal.ppat.1002844", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "sgr"=>"84866165048", "pmid"=>"22876183"}, "id"=>"5b315cd5-263e-3734-a957-072f225804c6", "abstract"=>"Wolbachia are widespread endosymbionts found in a large variety of arthropods. While these bacteria are generally transmitted vertically and exhibit weak virulence in their native hosts, a growing number of studies suggests that horizontal transfers of Wolbachia to new host species also occur frequently in nature. In transfer situations, virulence variations can be predicted since hosts and symbionts are not adapted to each other. Here, we describe a situation where a Wolbachia strain (wVulC) becomes a pathogen when transfected from its native terrestrial isopod host species (Armadillidium vulgare) to another species (Porcellio d. dilatatus). Such transfer of wVulC kills all recipient animals within 75 days. Before death, animals suffer symptoms such as growth slowdown and nervous system disorders. Neither those symptoms nor mortalities were observed after injection of wVulC into its native host A. vulgare. Analyses of wVulC's densities in main organs including Central Nervous System (CNS) of both naturally infected A. vulgare and transfected P. d. dilatatus and A. vulgare individuals revealed a similar pattern of host colonization suggesting an overall similar resistance of both host species towards this bacterium. However, for only P. d. dilatatus, we observed drastic accumulations of autophagic vesicles and vacuoles in the nerve cells and adipocytes of the CNS from individuals infected by wVulC. The symptoms and mortalities could therefore be explained by this huge autophagic response against wVulC in P. d. dilatatus cells that is not triggered in A. vulgare. Our results show that Wolbachia (wVulC) can lead to a pathogenic interaction when transferred horizontally into species that are phylogenetically close to their native hosts. This change in virulence likely results from the autophagic response of the host, strongly altering its tolerance to the symbiont and turning it into a deadly pathogen.", "link"=>"http://www.mendeley.com/research/high-virulence-wolbachia-after-host-switching-autophagy-hurts", "reader_count"=>66, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>12, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>12, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>4, "Biochemistry, Genetics and Molecular Biology"=>3, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>51, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>51}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>4}}, "reader_count_by_country"=>{"Netherlands"=>1, "Belgium"=>1, "United States"=>1, "Brazil"=>3, "Germany"=>2}, "group_count"=>2}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/598641"], "description"=>"<p>(A) Comparison between (i) <i>P. d. dilatatus</i> in dark grey and <i>A. vulgare</i> in white injected with <i>w</i>VulC and (ii) naturally infected <i>A. vulgare</i> in light grey revealed no significant differences for the <i>Wolbachia</i> loads in CNS cells, gonads and hemocytes (<i>i.e</i> immune cells), at both 30 and 60 days post-injection. (B) Comparison between (i) <i>P. d. dilatatus</i> in dark grey and <i>A. vulgare</i> in white injected with <i>w</i>Dil and (ii) naturally infected <i>P. d. dilatatus</i> in dim grey revealed no significant differences for the <i>Wolbachia</i> loads in CNS cells at both 30 and 60 days PI. However, at 60 days post-injection, for gonads and hemocytes <i>w</i>Dil loads were significantly higher in the native host <i>P. d. dilatatus</i> than in <i>A. vulgare</i>. A global comparison between <i>w</i>Dil and <i>w</i>VulC loads showed that <i>w</i>VulC (A) always exhibited higher bacterial loads than <i>w</i>Dil (B) in both host species.</p>", "links"=>[], "tags"=>["loads", "gonads", "hemocytes"], "article_id"=>269132, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844.g003", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Wolbachia_loads_in_CNS_gonads_and_hemocytes_of_Porcellio_d_dilatatus_and_Armadillidium_vulgare_/269132", "title"=>"<i>Wolbachia</i> loads in CNS, gonads and hemocytes of <i>Porcellio d. dilatatus</i> and <i>Armadillidium vulgare</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-02 02:32:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/599009"], "description"=>"<p>These adipocytes are localised around the nerve cells of the CNS and constitutes the sheathing of this organ. (A) At 30 days post-injection, autolysosomes, autophagosomes but also bacteria were observed: autophagic process was already higher compared to the control (Ad: adipocyte, Ap: Autophagosomes (Autophagic hallmark), Al: Autolysosomes, Wo: <i>Wolbachia</i>, Arrow head: magnified area). (B) At 60 days post-injection, the adipocytes were severely damaged by the accumulation of autophagic vesicles (Ad: adipocyte, Ap: Autophagosomes, Al: Autolysosomes, Wo: <i>Wolbachia</i>, Arrow head: magnified area). (C) With the antibody labelling anti-LC3B, the protein LC3B implicated in autophagic processes was detected in adipocytes of <i>P. d. dilatatus</i> injected with wVulC at 45 days post-injection. The highly labeled spherical structures would reflect the incorporation of the LC3B protein in the phagophores. (D) With adipocytes of <i>P. d. dilatatus</i> injected by <i>w</i>Dil but also in other tested situations, only really few of these structures were detected by epiflorescent microscopy.</p>", "links"=>[], "tags"=>["lc3b", "antibody", "labelling", "adipocytes", "cells"], "article_id"=>269492, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844.g005", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Micrograph_and_LC3B_antibody_labelling_of_adipocytes_neighboring_the_nerve_cells_of_Porcellio_d_dilatatus_/269492", "title"=>"Micrograph and LC3B antibody labelling of adipocytes neighboring the nerve cells of <i>Porcellio d. dilatatus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-02 02:38:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/598533"], "description"=>"<p>Animals were injected by pure suspension of <i>w</i>VulC, diluted <i>w</i>VulC inoculum (only for females), <i>w</i>Dil or control treatment and monitored during 75 days post-injection. (A) Gain of weight: Both <i>Wolbachia</i> strains negatively impact this parameter compared to the control treatment. However, <i>w</i>VulC (<i>i.e</i> pure or 1/100 diluted inoculum) induces a lower growth rate than the native strain <i>w</i>Dil. (B) Mobility: this parameter is dramatically reduced for animals injected by <i>w</i>VulC compared to those from other treatments. On the opposite, injection of <i>w</i>Dil has no significant effect on the host's mobility. (C) Burying behaviour: The level 0 corresponds to the surface of the substrate, negative values correspond to the number of buried animals while positive values correspond to the number of animals found at the surface of the substrate. For control treatment animals, not a single individual rose up at the surface and for individuals injected by <i>w</i>Dil only few animals were spotted at the surface. When inoculated by <i>w</i>VulC, all animals rose up to the substrate after 60 days. (D) Survival (a) data for females and (b) data for males: The injection of <i>w</i>VulC kills all the individuals. However, the males die quicker than the females. No extra-mortalities were reported for injection with <i>w</i>Dil compared to control treatment.</p>", "links"=>[], "tags"=>["plots"], "article_id"=>269026, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844.g002", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gain_of_weight_mobility_burying_survival_plots_for_Porcellio_dilatatus_/269026", "title"=>"Gain of weight, mobility, burying, survival plots for <i>Porcellio dilatatus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-02 02:30:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/599177"], "description"=>"<p>The gain of weight and mobility were compared between treatments at 60 days post-injection with a Gaussian linear mixed-effects model with randomized block effect fitted by maximum likelihood (ML). Survival curves obtained with the different treatments were compared using a general mixed-effects Cox model with randomized block effect.</p>", "links"=>[], "tags"=>["analyses", "ran", "injected"], "article_id"=>269661, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844.t001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistical_analyses_ran_on_the_life_history_traits_data_obtained_for_female_A_vulgare_injected_by_w_VulC_w_Dil_and_control_treatment_/269661", "title"=>"Statistical analyses ran on the life history traits data obtained for female <i>A. vulgare</i> injected by <i>w</i>VulC, <i>w</i>Dil and control treatment.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-08-02 02:41:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/598402"], "description"=>"<p>There were no significant differences between animals injected with <i>w</i>VulC, <i>w</i>Dil or control treatment for all these life history traits: Survival (A), Gain of weight (B) and Mobility (C).</p>", "links"=>[], "tags"=>["mobility", "plots", "75", "days"], "article_id"=>268892, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844.g001", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Survival_gain_of_weight_and_mobility_plots_for_Armadillidium_vulgare_during_75_days_post_injection_/268892", "title"=>"Survival, gain of weight and mobility plots for <i>Armadillidium vulgare</i> during 75 days post-injection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-02 02:28:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/313445"], "description"=>"<div><p><em>Wolbachia</em> are widespread endosymbionts found in a large variety of arthropods. While these bacteria are generally transmitted vertically and exhibit weak virulence in their native hosts, a growing number of studies suggests that horizontal transfers of <em>Wolbachia</em> to new host species also occur frequently in nature. In transfer situations, virulence variations can be predicted since hosts and symbionts are not adapted to each other. Here, we describe a situation where a <em>Wolbachia</em> strain (<em>w</em>VulC) becomes a pathogen when transfected from its native terrestrial isopod host species (<em>Armadillidium vulgare</em>) to another species (<em>Porcellio d. dilatatus</em>). Such transfer of <em>w</em>VulC kills all recipient animals within 75 days. Before death, animals suffer symptoms such as growth slowdown and nervous system disorders. Neither those symptoms nor mortalities were observed after injection of <em>w</em>VulC into its native host <em>A. vulgare</em>. Analyses of <em>w</em>VulC's densities in main organs including Central Nervous System (CNS) of both naturally infected <em>A. vulgare</em> and transfected <em>P. d. dilatatus</em> and <em>A. vulgare</em> individuals revealed a similar pattern of host colonization suggesting an overall similar resistance of both host species towards this bacterium. However, for only <em>P. d. dilatatus</em>, we observed drastic accumulations of autophagic vesicles and vacuoles in the nerve cells and adipocytes of the CNS from individuals infected by <em>w</em>VulC. The symptoms and mortalities could therefore be explained by this huge autophagic response against <em>w</em>VulC in <em>P. d. dilatatus</em> cells that is not triggered in <em>A. vulgare</em>. Our results show that <em>Wolbachia</em> (<em>w</em>VulC) can lead to a pathogenic interaction when transferred horizontally into species that are phylogenetically close to their native hosts. This change in virulence likely results from the autophagic response of the host, strongly altering its tolerance to the symbiont and turning it into a deadly pathogen.</p> </div>", "links"=>[], "tags"=>["virulence", "autophagy", "hurts"], "article_id"=>121826, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844", "stats"=>{"downloads"=>1, "page_views"=>76, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/High_Virulence_of_Wolbachia_after_Host_Switching_When_Autophagy_Hurts/121826", "title"=>"High Virulence of <em>Wolbachia</em> after Host Switching: When Autophagy Hurts", "pos_in_sequence"=>0, "defined_type"=>2, "published_date"=>"2012-08-02 00:30:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/599213"], "description"=>"<p>The gain of weight and mobility were compared between treatments at 60 days post-injection with a Gaussian linear mixed-effects model with randomized block effect fitted by maximum likelihood (ML). For comparison of the <i>P. d. dilatatus</i> location in boxes between treatments through the whole experiment, a generalized linear model with binomial error and logit link function was performed. Survival curves were compared using a general mixed-effects Cox model with randomized block effect as for <i>A. vulgare</i>.</p>", "links"=>[], "tags"=>["analyses", "ran", "injected", "diluted"], "article_id"=>269701, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844.t002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistical_analyses_ran_on_the_life_history_traits_data_obtained_for_P_d_dilatatus_injected_by_w_VulC_pure_and_diluted_inoculum_w_Dil_and_control_treatment_/269701", "title"=>"Statistical analyses ran on the life history traits data obtained for <i>P. d. dilatatus</i> injected by <i>w</i>VulC (pure and diluted inoculum), <i>w</i>Dil and control treatment.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-08-02 02:41:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/598820"], "description"=>"<p>These cells are localised in the CNS ganglion. (A) At 30 days post-injection, some autolysosomes and bacteria are visible: autophagic process is already quite high compared to control [N: Nucleus, V: Vacuole, Ap: Autophagosomes (Autophagic hallmark), Al: Autolysosomes, Wo: <i>Wolbachia</i>, *: a <i>Wolbachia</i> which seems to be surrounded by an autolysosome, Arrow head: magnified area]. (B) At 60 days post-injection, the nerve cells are severely damaged by the accumulation of autophagic vesicles (N: Nucleus, V: Vacuole, Ap: Autophagosomes (Autophagic hallmark), Al: Autolysosomes, Arrow head: magnified area and probably a <i>Wolbachia</i> in autophagic degradation).</p>", "links"=>[], "tags"=>["cells", "injected"], "article_id"=>269316, "categories"=>["Ecology", "Neuroscience", "Genetics", "Immunology", "Evolutionary Biology"], "users"=>["Winka Le Clec'h", "Christine Braquart-Varnier", "Maryline Raimond", "Jean-Baptiste Ferdy", "Didier Bouchon", "Mathieu Sicard"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002844.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Micrograph_of_nerve_cells_of_Porcellio_d_dilatatus_injected_by_w_VulC_/269316", "title"=>"Micrograph of nerve cells of <i>Porcellio d. dilatatus</i> injected by <i>w</i>VulC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-02 02:35:16"}

PMC Usage Stats | Further Information

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