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Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria

Invasive species could benefit from being introduced to locations with more favorable species interactions, including the loss of enemies, the gain of mutualists, or the simplification of complex interaction networks. Microbiomes are an important source of species interactions with strong fitness ef...

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Autores principales: Lu-Irving, Patricia, Harenčár, Julia G., Sounart, Hailey, Welles, Shana R., Swope, Sarah M., Baltrus, David A., Dlugosch, Katrina M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6403453/
https://www.ncbi.nlm.nih.gov/pubmed/30842267
http://dx.doi.org/10.1128/mSphere.00088-19
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author Lu-Irving, Patricia
Harenčár, Julia G.
Sounart, Hailey
Welles, Shana R.
Swope, Sarah M.
Baltrus, David A.
Dlugosch, Katrina M.
author_facet Lu-Irving, Patricia
Harenčár, Julia G.
Sounart, Hailey
Welles, Shana R.
Swope, Sarah M.
Baltrus, David A.
Dlugosch, Katrina M.
author_sort Lu-Irving, Patricia
collection PubMed
description Invasive species could benefit from being introduced to locations with more favorable species interactions, including the loss of enemies, the gain of mutualists, or the simplification of complex interaction networks. Microbiomes are an important source of species interactions with strong fitness effects on multicellular organisms, and these interactions are known to vary across regions. The highly invasive plant yellow starthistle (Centaurea solstitialis) has been shown to experience more favorable microbial interactions in its invasions of the Americas, but the microbiome that must contribute to this variation in interactions is unknown. We sequenced amplicons of 16S rRNA genes to characterize bacterial community compositions in the phyllosphere, ectorhizosphere, and endorhizosphere of yellow starthistle plants from seven invading populations in California, USA, and eight native populations in Europe. We tested for the differentiation of microbiomes by geography, plant compartment, and plant genotype. Bacterial communities differed significantly between native and invading plants within plant compartments, with consistently lower diversity in the microbiome of invading plants. The diversity of bacteria in roots was positively correlated with plant genotype diversity within both ranges, but this relationship did not explain microbiome differences between ranges. Our results reveal that these invading plants are experiencing either a simplified microbial environment or simplified microbial interactions as a result of the dominance of a few taxa within their microbiome. Our findings highlight several alternative hypotheses for the sources of variation that we observe in invader microbiomes and the potential for altered bacterial interactions to facilitate invasion success. IMPORTANCE Previous studies have found that introduced plants commonly experience more favorable microbial interactions in their non-native range, suggesting that changes to the microbiome could be an important contributor to invasion success. Little is known about microbiome variation across native and invading populations, however, and the potential sources of more favorable interactions are undescribed. Here, we report one of the first microbiome comparisons of plants from multiple native and invading populations, in the noxious weed yellow starthistle. We identify clear differences in composition and diversity of microbiome bacteria. Our findings raise new questions about the sources of these differences, and we outline the next generation of research that will be required to connect microbiome variation to its potential role in plant invasions.
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spelling pubmed-64034532019-03-12 Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria Lu-Irving, Patricia Harenčár, Julia G. Sounart, Hailey Welles, Shana R. Swope, Sarah M. Baltrus, David A. Dlugosch, Katrina M. mSphere Research Article Invasive species could benefit from being introduced to locations with more favorable species interactions, including the loss of enemies, the gain of mutualists, or the simplification of complex interaction networks. Microbiomes are an important source of species interactions with strong fitness effects on multicellular organisms, and these interactions are known to vary across regions. The highly invasive plant yellow starthistle (Centaurea solstitialis) has been shown to experience more favorable microbial interactions in its invasions of the Americas, but the microbiome that must contribute to this variation in interactions is unknown. We sequenced amplicons of 16S rRNA genes to characterize bacterial community compositions in the phyllosphere, ectorhizosphere, and endorhizosphere of yellow starthistle plants from seven invading populations in California, USA, and eight native populations in Europe. We tested for the differentiation of microbiomes by geography, plant compartment, and plant genotype. Bacterial communities differed significantly between native and invading plants within plant compartments, with consistently lower diversity in the microbiome of invading plants. The diversity of bacteria in roots was positively correlated with plant genotype diversity within both ranges, but this relationship did not explain microbiome differences between ranges. Our results reveal that these invading plants are experiencing either a simplified microbial environment or simplified microbial interactions as a result of the dominance of a few taxa within their microbiome. Our findings highlight several alternative hypotheses for the sources of variation that we observe in invader microbiomes and the potential for altered bacterial interactions to facilitate invasion success. IMPORTANCE Previous studies have found that introduced plants commonly experience more favorable microbial interactions in their non-native range, suggesting that changes to the microbiome could be an important contributor to invasion success. Little is known about microbiome variation across native and invading populations, however, and the potential sources of more favorable interactions are undescribed. Here, we report one of the first microbiome comparisons of plants from multiple native and invading populations, in the noxious weed yellow starthistle. We identify clear differences in composition and diversity of microbiome bacteria. Our findings raise new questions about the sources of these differences, and we outline the next generation of research that will be required to connect microbiome variation to its potential role in plant invasions. American Society for Microbiology 2019-03-06 /pmc/articles/PMC6403453/ /pubmed/30842267 http://dx.doi.org/10.1128/mSphere.00088-19 Text en Copyright © 2019 Lu-Irving et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Lu-Irving, Patricia
Harenčár, Julia G.
Sounart, Hailey
Welles, Shana R.
Swope, Sarah M.
Baltrus, David A.
Dlugosch, Katrina M.
Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria
title Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria
title_full Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria
title_fullStr Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria
title_full_unstemmed Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria
title_short Native and Invading Yellow Starthistle (Centaurea solstitialis) Microbiomes Differ in Composition and Diversity of Bacteria
title_sort native and invading yellow starthistle (centaurea solstitialis) microbiomes differ in composition and diversity of bacteria
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6403453/
https://www.ncbi.nlm.nih.gov/pubmed/30842267
http://dx.doi.org/10.1128/mSphere.00088-19
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