The Relationship Between Microbiomes and Selective Regimes in the Sponge Genus Ircinia

Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns...

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Published inFrontiers in microbiology Vol. 12; p. 607289
Main Authors Kelly, Joseph B, Carlson, David E, Low, Jun Siong, Rice, Tyler, Thacker, Robert W
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 11.03.2021
Subjects
16S metabarcoding
innate immunity
Microbiology
microbiome
RADseq
sponge (Porifera)
RADseq
sponge (Porifera)
16S metabarcoding
innate immunity
microbiome
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Abstract Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns of selection in the host sponges' genomes that underlie tolerance and control of their microbiomes are still poorly understood. To elucidate these patterns of selection, we performed a population genetic analysis on multiple species of from Belize, Florida, and Panama using an -outlier approach on transcriptome-annotated RADseq loci. As part of the analysis, we delimited species boundaries among seven growth forms of . Our analyses identified balancing selection in immunity genes that have implications for the hosts' tolerance of high densities of microbes. Additionally, our results support the hypothesis that each of the seven growth forms constitutes a distinct species that is characterized by a unique microbiome. These results illuminate the evolutionary pathways that promote stable associations between host sponges and their microbiomes, and that potentially facilitate ecological divergence among species.
AbstractList Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns of selection in the host sponges’ genomes that underlie tolerance and control of their microbiomes are still poorly understood. To elucidate these patterns of selection, we performed a population genetic analysis on multiple species of Ircinia from Belize, Florida, and Panama using an FST-outlier approach on transcriptome-annotated RADseq loci. As part of the analysis, we delimited species boundaries among seven growth forms of Ircinia. Our analyses identified balancing selection in immunity genes that have implications for the hosts’ tolerance of high densities of microbes. Additionally, our results support the hypothesis that each of the seven growth forms constitutes a distinct Ircinia species that is characterized by a unique microbiome. These results illuminate the evolutionary pathways that promote stable associations between host sponges and their microbiomes, and that potentially facilitate ecological divergence among Ircinia species.
Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns of selection in the host sponges' genomes that underlie tolerance and control of their microbiomes are still poorly understood. To elucidate these patterns of selection, we performed a population genetic analysis on multiple species of from Belize, Florida, and Panama using an -outlier approach on transcriptome-annotated RADseq loci. As part of the analysis, we delimited species boundaries among seven growth forms of . Our analyses identified balancing selection in immunity genes that have implications for the hosts' tolerance of high densities of microbes. Additionally, our results support the hypothesis that each of the seven growth forms constitutes a distinct species that is characterized by a unique microbiome. These results illuminate the evolutionary pathways that promote stable associations between host sponges and their microbiomes, and that potentially facilitate ecological divergence among species.
Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns of selection in the host sponges’ genomes that underlie tolerance and control of their microbiomes are still poorly understood. To elucidate these patterns of selection, we performed a population genetic analysis on multiple species of Ircinia from Belize, Florida, and Panama using an F ST -outlier approach on transcriptome-annotated RADseq loci. As part of the analysis, we delimited species boundaries among seven growth forms of Ircinia . Our analyses identified balancing selection in immunity genes that have implications for the hosts’ tolerance of high densities of microbes. Additionally, our results support the hypothesis that each of the seven growth forms constitutes a distinct Ircinia species that is characterized by a unique microbiome. These results illuminate the evolutionary pathways that promote stable associations between host sponges and their microbiomes, and that potentially facilitate ecological divergence among Ircinia species.
Author Low, Jun Siong
Rice, Tyler
Carlson, David E
Kelly, Joseph B
Thacker, Robert W
AuthorAffiliation 4 Department of Immunobiology, Yale University School of Medicine , New Haven, CT , United States
1 Department of Ecology and Evolution, Stony Brook University , Stony Brook, NY , United States
2 Limnological Institute University Konstanz, Aquatic Ecology and Evolution , Konstanz , Germany
5 Smithsonian Tropical Research Institute , Balboa , Panama
3 Institute for Research in Biomedicine, Università della Svizzera Italiana , Bellinzona , Switzerland
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Keywords RADseq
sponge (Porifera)
16S metabarcoding
innate immunity
microbiome
Language English
License Copyright © 2021 Kelly, Carlson, Low, Rice and Thacker.
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Notes Edited by: Zhiyong Li, Shanghai Jiao Tong University, China
This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology
Reviewed by: Matthew Agler, Friedrich Schiller University Jena, Germany; Lucia Pita, GEOMAR Helmholtz Center for Ocean Research Kiel, Germany
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Snippet Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must...
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SubjectTerms 16S metabarcoding
innate immunity
Microbiology
microbiome
RADseq
sponge (Porifera)
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Title The Relationship Between Microbiomes and Selective Regimes in the Sponge Genus Ircinia
URI https://www.ncbi.nlm.nih.gov/pubmed/33776953
https://pubmed.ncbi.nlm.nih.gov/PMC7990798
https://doaj.org/article/b7a9fb23065045c8ad2e200cf613abfa
Volume 12
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