Hannah E Epstein, Tanya Brown, Ayọmikun O Akinrinade, Ryan McMinds, F Joseph Pollock, Dylan Sonett, Styles Smith, David G Bourne, Carolina S Carpenter, Rob Knight, Bette L Willis, Mónica Medina, Joleah B Lamb, Rebecca Vega Thurber, Jesse R Zaneveld
{"title":"在珊瑚进化过程中,微生物介导的生长和防御之间权衡的证据。","authors":"Hannah E Epstein, Tanya Brown, Ayọmikun O Akinrinade, Ryan McMinds, F Joseph Pollock, Dylan Sonett, Styles Smith, David G Bourne, Carolina S Carpenter, Rob Knight, Bette L Willis, Mónica Medina, Joleah B Lamb, Rebecca Vega Thurber, Jesse R Zaneveld","doi":"10.1186/s42523-024-00370-z","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea.</p><p><strong>Results: </strong>Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the \"Global Coral Microbiome Project\") and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates.</p><p><strong>Conclusions: </strong>These results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs.</p>","PeriodicalId":72201,"journal":{"name":"Animal microbiome","volume":"7 1","pages":"1"},"PeriodicalIF":4.9000,"publicationDate":"2025-01-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11697511/pdf/","citationCount":"0","resultStr":"{\"title\":\"Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution.\",\"authors\":\"Hannah E Epstein, Tanya Brown, Ayọmikun O Akinrinade, Ryan McMinds, F Joseph Pollock, Dylan Sonett, Styles Smith, David G Bourne, Carolina S Carpenter, Rob Knight, Bette L Willis, Mónica Medina, Joleah B Lamb, Rebecca Vega Thurber, Jesse R Zaneveld\",\"doi\":\"10.1186/s42523-024-00370-z\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea.</p><p><strong>Results: </strong>Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the \\\"Global Coral Microbiome Project\\\") and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates.</p><p><strong>Conclusions: </strong>These results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs.</p>\",\"PeriodicalId\":72201,\"journal\":{\"name\":\"Animal microbiome\",\"volume\":\"7 1\",\"pages\":\"1\"},\"PeriodicalIF\":4.9000,\"publicationDate\":\"2025-01-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11697511/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Animal microbiome\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1186/s42523-024-00370-z\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Animal microbiome","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1186/s42523-024-00370-z","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
Evidence for microbially-mediated tradeoffs between growth and defense throughout coral evolution.
Background: Evolutionary tradeoffs between life-history strategies are important in animal evolution. Because microbes can influence multiple aspects of host physiology, including growth rate and susceptibility to disease or stress, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a biodiverse, data-rich, and ecologically-relevant host system to explore this idea.
Results: Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by conducting a cross-species coral microbiome survey (the "Global Coral Microbiome Project") and combining the results with long-term global disease prevalence and coral trait data. Interpreting these data in their phylogenetic context, we show that microbial dominance predicts disease susceptibility, and traced this dominance-disease association to a single putatively beneficial symbiont genus, Endozoicomonas. Endozoicomonas relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera, while also correlating strongly with high growth rates.
Conclusions: These results demonstrate that the evolution of Endozoicomonas symbiosis in corals correlates with both disease prevalence and growth rate, and suggest a mediating role. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbioses influence animal life-history tradeoffs.