Multifaceted Defense against Antagonistic Microbes in Developing Offspring of the Parasitoid Wasp Ampulex compressa (Hymenoptera, Ampulicidae)
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{"title"=>"Multifaceted defense against antagonistic microbes in developing offspring of the parasitoid wasp Ampulex compressa (Hymenoptera, Ampulicidae)", "type"=>"journal", "authors"=>[{"first_name"=>"Katharina", "last_name"=>"Weiss", "scopus_author_id"=>"55994785400"}, {"first_name"=>"Christopher", "last_name"=>"Parzefall", "scopus_author_id"=>"55569285700"}, {"first_name"=>"Gudrun", "last_name"=>"Herzner", "scopus_author_id"=>"8316712400"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"24886721", "sgr"=>"84902322571", "doi"=>"10.1371/journal.pone.0098784", "scopus"=>"2-s2.0-84902322571", "pui"=>"373302339", "issn"=>"19326203"}, "id"=>"1f0d113d-e03d-3f3e-b793-33f76e7c0807", "abstract"=>"Effective antimicrobial strategies are essential adaptations of insects to protect themselves, their offspring, and their foods from microbial pathogens and decomposers. Larvae of the emerald cockroach wasp, Ampulex compressa, sanitize their cockroach hosts, Periplaneta americana, with a cocktail of nine antimicrobials comprising mainly (R)-(-)-mellein and micromolide. The blend of these antimicrobials has broad-spectrum antimicrobial activity. Here we explore the spatio-temporal pattern of deployment of antimicrobials during the development from egg to adult as well as their physico-chemical properties to assess how these aspects may contribute to the success of the antimicrobial strategy. Using gas chromatography/mass spectrometry (GC/MS) we show that larvae start sanitizing their food as soon as they have entered their host to feed on its tissue. Subsequently, they impregnate the cockroach carcass with antimicrobials to create a hygienic substrate for cocoon spinning inside the host. Finally, the antimicrobials are incorporated into the cocoon. The antimicrobial profiles on cockroach and wasp cocoon differed markedly. While micromolide persisted on the cockroaches until emergence of the wasps, solid-phase microextraction sampling and GC/MS analysis revealed that (R)-(-)-mellein vaporized from the cockroaches and accumulated in the enclosed nest. In microbial challenge assays (R)-(-)-mellein in the headspace of parasitized cockroaches inhibited growth of entomopathogenic and opportunistic microbes (Serratia marcescens, Aspergillus sydowii, Metarhizium brunneum). We conclude that, in addition to food sanitation, A. compressa larvae enclose themselves in two defensive walls by impregnating the cocoon and the cockroach cuticle with antimicrobials. On top of that, they use vaporous (R)-(-)-mellein to sanitize the nest by fumigation. This multifaceted antimicrobial defense strategy involving the spatially and temporally coordinated deployment of several antimicrobials in solution and vapor form has apparently evolved to reliably protect the larvae themselves and their food against a broad range of antagonistic microbes.", "link"=>"http://www.mendeley.com/research/multifaceted-defense-against-antagonistic-microbes-developing-offspring-parasitoid-wasp-ampulex-comp", "reader_count"=>16, "reader_count_by_academic_status"=>{"Student > Doctoral Student"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>4}, "reader_count_by_user_role"=>{"Student > Doctoral Student"=>2, "Researcher"=>5, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>4}, "reader_count_by_subject_area"=>{"Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>12, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>12}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Brazil"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1516864"], "description"=>"<p>Total ion chromatograms of (A) a solvent extract of a parasitized <i>P. americana</i> cockroach, (B) a solvent extract of a cocoon of <i>A. compressa</i>, and (C) a headspace sample of a parasitized <i>P. americana</i> cockroach obtained by solid-phase microextraction. Although the relative amounts of compounds in solvent extract showed a broad variation, the chromatograms can be considered typical. The peaks of minor compounds may not be visible due to the magnification used. Peak numbers correspond to the numbers in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098784#pone-0098784-t001\" target=\"_blank\">Table 1</a>, Peak 3 =  (<i>R</i>)-(-)-mellein, Peak 23 =  micromolide. IS: internal standard.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "profiles", "parasitized"], "article_id"=>1042601, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.g001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemical_profiles_of_parasitized_P_americana_and_A_compressa_cocoons_/1042601", "title"=>"Chemical profiles of parasitized <i>P. americana</i> and <i>A. compressa</i> cocoons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516865"], "description"=>"<p>Two-dimensional MDS representation of the chemical profiles of parasitized <i>P. americana</i> cockroaches (black dots) and <i>A. compressa</i> wasp cocoons (green diamonds) (stress value: 0.03). The 95% concentration ellipses depict the regions where 95% of the points of the respective group are expected to fall.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "profiles", "cockroaches"], "article_id"=>1042602, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_the_chemical_profiles_of_cockroaches_and_cocoons_/1042602", "title"=>"Comparison of the chemical profiles of cockroaches and cocoons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516866"], "description"=>"<p>Median amounts of (A) all larval substances, (B) micromolide, and (C) mellein found in parasitized cockroaches of different developmental stages (<i>n</i> = 9, 10, 11, 10, 10, 9, 10; see also <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098784#pone.0098784.s002\" target=\"_blank\">Figure S2</a>). Horizontal line inside box: median, box: 25–75 percent quartiles, whiskers: minimal and maximal values. Groups that do not share at least one letter above the boxplot are significantly different. For levels of significance of the pairwise comparisons see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098784#pone.0098784.s007\" target=\"_blank\">Tables S2</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098784#pone.0098784.s008\" target=\"_blank\">S3</a>.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "larval", "antimicrobials"], "article_id"=>1042603, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.g003", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Temporal_changes_in_the_amount_of_larval_antimicrobials_in_A_compressa_nests_/1042603", "title"=>"Temporal changes in the amount of larval antimicrobials in <i>A. compressa</i> nests.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516867"], "description"=>"<p>Relative amounts of mellein (black) and micromolide (blue) found on parasitized cockroaches during the development of <i>A. compressa</i>. Shown are means ± one standard deviation.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "amounts"], "article_id"=>1042604, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Temporal_changes_in_relative_amounts_of_major_compounds_/1042604", "title"=>"Temporal changes in relative amounts of major compounds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516868"], "description"=>"<p>(A) Reddish bacterial colonies on a control agar cube, (B) whitish bacterial colonies on an agar cube incubated in the headspace of a cockroach parasitized by <i>A. compressa</i>. (C, D) Median amount of bacteria found in (C) samples taken from control agar cubes and agar cubes incubated in the headspace of parasitized cockroaches (<i>n</i> = 10 each) and (D) samples taken from control agar cubes and agar cubes incubated in the headspace of a filter paper impregnated with synthetic mellein (<i>n</i> = 10 each). Horizontal line inside box: median, box: 25–75 percent quartiles, whiskers: minimal and maximal values.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "volatile", "antimicrobials"], "article_id"=>1042605, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.g005", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_volatile_antimicrobials_on_S_marcescens_/1042605", "title"=>"Effect of volatile antimicrobials on <i>S. marcescens</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516869"], "description"=>"<p><i>A. sydowii</i>: (A) control agar cube, (B) agar cube incubated in the headspace of a parasitized cockroach, (E) control agar cube, (F) agar cube incubated in the headspace of a filter paper impregnated with synthetic mellein. <i>M. brunneum</i>: (C) control agar cube, (D) agar cube incubated in the headspace of a parasitized cockroach, (G) control agar cube, and (H) agar cube incubated in the headspace of filter paper impregnated with synthetic mellein. All cubes were approximately 1×1×0.5 cm in size.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "volatile", "compounds"], "article_id"=>1042606, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.g006", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_volatile_compounds_on_A_sydowii_and_M_brunneum_/1042606", "title"=>"Effect of volatile compounds on <i>A. sydowii</i> and <i>M. brunneum</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516870"], "description"=>"<p>(A) Control agar cube and (B) agar cube incubated in the headspace of a parasitized cockroach (agar cubes were approximately 1×1×0.5 cm in size; magnifications of photographs are equal).</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "volatile", "compounds"], "article_id"=>1042607, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.g007", "stats"=>{"downloads"=>2, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_volatile_compounds_on_A_nomius_/1042607", "title"=>"Effect of volatile compounds on <i>A. nomius</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516871"], "description"=>"<p>Portions of the agar surfaces overgrown by <i>A. sydowii</i> or <i>M. brunneum</i> (median ± median absolute deviation) after incubation in the headspace of parasitized cockroaches or filter papers impregnated with synthetic mellein and the respective controls. For <i>A. nomius</i> the total areas of mycelial growth (median ± median absolute deviation) are shown (see text for further details).</p><p><i>n</i> = 5 for all groups.</p>#<p>Mann-Whitney <i>U</i> test: <i>df</i> = 1, exact <i>p</i> = 0.008.</p>##<p>Mann-Whitney U test: <i>df</i> = 1, exact <i>p</i> = 0.02.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "antifungal"], "article_id"=>1042608, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.t002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_the_antifungal_challenge_assays_/1042608", "title"=>"Results of the antifungal challenge assays.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516872"], "description"=>"<p>Chemical composition of solvent extracts of parasitized <i>P. americana</i> cockroaches and <i>A. compressa</i> cocoons as well as mean amounts [µg] ± standard deviation of substances found in single extracts (<i>n</i> = 28). Compounds derived from <i>A. compressa</i> larvae (‘larval substances’) are in boldface type.</p><p>LRI =  linear retention index (calculated in relation to <i>n</i>-alkanes) on a RH-5ms+ column.</p><p>*Identified by comparing mass spectrum and retention time with a synthetic reference compound.</p><p>All other compounds were identified by comparison with data from earlier analyses <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098784#pone.0098784-Herzner1\" target=\"_blank\">[1]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098784#pone.0098784-Herzner3\" target=\"_blank\">[53]</a>.</p>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "compounds", "cockroaches"], "article_id"=>1042609, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098784.t001", "stats"=>{"downloads"=>5, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_chemical_compounds_on_cockroaches_and_cocoons_/1042609", "title"=>"List of chemical compounds on cockroaches and cocoons.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-02 04:30:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1516873", "https://ndownloader.figshare.com/files/1516874", "https://ndownloader.figshare.com/files/1516875", "https://ndownloader.figshare.com/files/1516876", "https://ndownloader.figshare.com/files/1516877", "https://ndownloader.figshare.com/files/1516878", "https://ndownloader.figshare.com/files/1516879", "https://ndownloader.figshare.com/files/1516880", "https://ndownloader.figshare.com/files/1516881"], "description"=>"<div><p>Effective antimicrobial strategies are essential adaptations of insects to protect themselves, their offspring, and their foods from microbial pathogens and decomposers. Larvae of the emerald cockroach wasp, <i>Ampulex compressa</i>, sanitize their cockroach hosts, <i>Periplaneta americana</i>, with a cocktail of nine antimicrobials comprising mainly (<i>R</i>)-(-)-mellein and micromolide. The blend of these antimicrobials has broad-spectrum antimicrobial activity. Here we explore the spatio-temporal pattern of deployment of antimicrobials during the development from egg to adult as well as their physico-chemical properties to assess how these aspects may contribute to the success of the antimicrobial strategy. Using gas chromatography/mass spectrometry (GC/MS) we show that larvae start sanitizing their food as soon as they have entered their host to feed on its tissue. Subsequently, they impregnate the cockroach carcass with antimicrobials to create a hygienic substrate for cocoon spinning inside the host. Finally, the antimicrobials are incorporated into the cocoon. The antimicrobial profiles on cockroach and wasp cocoon differed markedly. While micromolide persisted on the cockroaches until emergence of the wasps, solid-phase microextraction sampling and GC/MS analysis revealed that (<i>R</i>)-(-)-mellein vaporized from the cockroaches and accumulated in the enclosed nest. In microbial challenge assays (<i>R</i>)-(-)-mellein in the headspace of parasitized cockroaches inhibited growth of entomopathogenic and opportunistic microbes (<i>Serratia marcescens</i>, <i>Aspergillus sydowii</i>, <i>Metarhizium brunneum</i>). We conclude that, in addition to food sanitation, <i>A. compressa</i> larvae enclose themselves in two defensive walls by impregnating the cocoon and the cockroach cuticle with antimicrobials. On top of that, they use vaporous (<i>R</i>)-(-)-mellein to sanitize the nest by fumigation. This multifaceted antimicrobial defense strategy involving the spatially and temporally coordinated deployment of several antimicrobials in solution and vapor form has apparently evolved to reliably protect the larvae themselves and their food against a broad range of antagonistic microbes.</p></div>", "links"=>[], "tags"=>["ecology", "Chemical ecology", "microbiology", "Zoology", "Entomology", "multifaceted", "antagonistic", "microbes", "offspring", "parasitoid", "wasp"], "article_id"=>1042610, "categories"=>["Biological Sciences", "Ecology"], "users"=>["Katharina Weiß", "Christopher Parzefall", "Gudrun Herzner"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0098784.s001", "https://dx.doi.org/10.1371/journal.pone.0098784.s002", "https://dx.doi.org/10.1371/journal.pone.0098784.s003", "https://dx.doi.org/10.1371/journal.pone.0098784.s004", "https://dx.doi.org/10.1371/journal.pone.0098784.s005", "https://dx.doi.org/10.1371/journal.pone.0098784.s006", "https://dx.doi.org/10.1371/journal.pone.0098784.s007", "https://dx.doi.org/10.1371/journal.pone.0098784.s008", "https://dx.doi.org/10.1371/journal.pone.0098784.s009"], "stats"=>{"downloads"=>26, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Multifaceted_Defense_against_Antagonistic_Microbes_in_Developing_Offspring_of_the_Parasitoid_Wasp_Ampulex_compressa_Hymenoptera_Ampulicidae_/1042610", "title"=>"Multifaceted Defense against Antagonistic Microbes in Developing Offspring of the Parasitoid Wasp <i>Ampulex compressa</i> (Hymenoptera, Ampulicidae)", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-06-02 04:30:24"}

PMC Usage Stats | Further Information

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Relative Metric

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