Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded Habitats

Massive fouling by the invasive ascidian <i>Ciona intestinalis</i> in Prince Edward Island (PEI, Canada) has been causing devastating losses to the local blue mussel farms. In order to gain first insights into so far unexplored factors that may contribute to the invasiveness of <i>...

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Main Authors: Caroline Utermann, Martina Blümel, Kathrin Busch, Larissa Buedenbender, Yaping Lin, Bradley A. Haltli, Russell G. Kerr, Elizabeta Briski, Ute Hentschel, Deniz Tasdemir
Format: Article
Language:English
Published: MDPI AG 2020-12-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/12/2022
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author Caroline Utermann
Martina Blümel
Kathrin Busch
Larissa Buedenbender
Yaping Lin
Bradley A. Haltli
Russell G. Kerr
Elizabeta Briski
Ute Hentschel
Deniz Tasdemir
author_facet Caroline Utermann
Martina Blümel
Kathrin Busch
Larissa Buedenbender
Yaping Lin
Bradley A. Haltli
Russell G. Kerr
Elizabeta Briski
Ute Hentschel
Deniz Tasdemir
author_sort Caroline Utermann
collection DOAJ
description Massive fouling by the invasive ascidian <i>Ciona intestinalis</i> in Prince Edward Island (PEI, Canada) has been causing devastating losses to the local blue mussel farms. In order to gain first insights into so far unexplored factors that may contribute to the invasiveness of <i>C. intestinalis</i> in PEI, we undertook comparative microbiome and metabolome studies on specific tissues from <i>C. intestinalis</i> populations collected in invaded (PEI) and native regions (Helgoland and Kiel, Germany). Microbial community analyses and untargeted metabolomics revealed clear location- and tissue-specific patterns showing that biogeography and the sampled tissue shape the microbiome and metabolome of <i>C. intestinalis</i>. Moreover, we observed higher microbial and chemical diversity in <i>C. intestinalis</i> from PEI than in the native populations. Bacterial OTUs specific to <i>C. intestinalis</i> from PEI included Cyanobacteria (e.g., <i>Leptolyngbya</i> sp.) and Rhodobacteraceae (e.g., <i>Roseobacter</i> sp.), while populations from native sampling sites showed higher abundances of e.g., Firmicutes (Helgoland) and Epsilonproteobacteria (Kiel). Altogether 121 abundant metabolites were putatively annotated in the global ascidian metabolome, of which 18 were only detected in the invasive PEI population (e.g., polyketides and terpenoids), while six (e.g., sphingolipids) or none were exclusive to the native specimens from Helgoland and Kiel, respectively. Some identified bacteria and metabolites reportedly possess bioactive properties (e.g., antifouling and antibiotic) that may contribute to the overall fitness of <i>C. intestinalis</i>. Hence, this first study provides a basis for future studies on factors underlying the global invasiveness of <i>Ciona</i> species.
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spelling doaj.art-50646f16e3dd47e09a62e429a599fac32023-11-21T01:16:02ZengMDPI AGMicroorganisms2076-26072020-12-01812202210.3390/microorganisms8122022Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded HabitatsCaroline Utermann0Martina Blümel1Kathrin Busch2Larissa Buedenbender3Yaping Lin4Bradley A. Haltli5Russell G. Kerr6Elizabeta Briski7Ute Hentschel8Deniz Tasdemir9GEOMAR Centre for Marine Biotechnology (GEOMAR-Biotech), Research Unit Marine Natural Products Chemistry, GEOMAR Helmholtz Centre for Ocean Research Kiel, Am Kiel-Kanal 44, 24106 Kiel, GermanyGEOMAR Centre for Marine Biotechnology (GEOMAR-Biotech), Research Unit Marine Natural Products Chemistry, GEOMAR Helmholtz Centre for Ocean Research Kiel, Am Kiel-Kanal 44, 24106 Kiel, GermanyResearch Unit Marine Symbioses, GEOMAR Helmholtz Centre for Ocean Research Kiel, Duesternbrooker Weg 20, 24105 Kiel, GermanyGEOMAR Centre for Marine Biotechnology (GEOMAR-Biotech), Research Unit Marine Natural Products Chemistry, GEOMAR Helmholtz Centre for Ocean Research Kiel, Am Kiel-Kanal 44, 24106 Kiel, GermanyResearch Group Invasion Ecology, Research Unit Experimental Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Duesternbrooker Weg 20, 24105 Kiel, GermanyDepartment of Chemistry, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE C1A 4P3, CanadaDepartment of Chemistry, University of Prince Edward Island, 550 University Avenue, Charlottetown, PE C1A 4P3, CanadaResearch Group Invasion Ecology, Research Unit Experimental Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Duesternbrooker Weg 20, 24105 Kiel, GermanyResearch Unit Marine Symbioses, GEOMAR Helmholtz Centre for Ocean Research Kiel, Duesternbrooker Weg 20, 24105 Kiel, GermanyGEOMAR Centre for Marine Biotechnology (GEOMAR-Biotech), Research Unit Marine Natural Products Chemistry, GEOMAR Helmholtz Centre for Ocean Research Kiel, Am Kiel-Kanal 44, 24106 Kiel, GermanyMassive fouling by the invasive ascidian <i>Ciona intestinalis</i> in Prince Edward Island (PEI, Canada) has been causing devastating losses to the local blue mussel farms. In order to gain first insights into so far unexplored factors that may contribute to the invasiveness of <i>C. intestinalis</i> in PEI, we undertook comparative microbiome and metabolome studies on specific tissues from <i>C. intestinalis</i> populations collected in invaded (PEI) and native regions (Helgoland and Kiel, Germany). Microbial community analyses and untargeted metabolomics revealed clear location- and tissue-specific patterns showing that biogeography and the sampled tissue shape the microbiome and metabolome of <i>C. intestinalis</i>. Moreover, we observed higher microbial and chemical diversity in <i>C. intestinalis</i> from PEI than in the native populations. Bacterial OTUs specific to <i>C. intestinalis</i> from PEI included Cyanobacteria (e.g., <i>Leptolyngbya</i> sp.) and Rhodobacteraceae (e.g., <i>Roseobacter</i> sp.), while populations from native sampling sites showed higher abundances of e.g., Firmicutes (Helgoland) and Epsilonproteobacteria (Kiel). Altogether 121 abundant metabolites were putatively annotated in the global ascidian metabolome, of which 18 were only detected in the invasive PEI population (e.g., polyketides and terpenoids), while six (e.g., sphingolipids) or none were exclusive to the native specimens from Helgoland and Kiel, respectively. Some identified bacteria and metabolites reportedly possess bioactive properties (e.g., antifouling and antibiotic) that may contribute to the overall fitness of <i>C. intestinalis</i>. Hence, this first study provides a basis for future studies on factors underlying the global invasiveness of <i>Ciona</i> species.https://www.mdpi.com/2076-2607/8/12/2022biological invasionascidian<i>Ciona intestinalis</i>Prince Edward Islandmicrobiomesymbionts
spellingShingle Caroline Utermann
Martina Blümel
Kathrin Busch
Larissa Buedenbender
Yaping Lin
Bradley A. Haltli
Russell G. Kerr
Elizabeta Briski
Ute Hentschel
Deniz Tasdemir
Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded Habitats
Microorganisms
biological invasion
ascidian
<i>Ciona intestinalis</i>
Prince Edward Island
microbiome
symbionts
title Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded Habitats
title_full Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded Habitats
title_fullStr Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded Habitats
title_full_unstemmed Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded Habitats
title_short Comparative Microbiome and Metabolome Analyses of the Marine Tunicate <i>Ciona intestinalis</i> from Native and Invaded Habitats
title_sort comparative microbiome and metabolome analyses of the marine tunicate i ciona intestinalis i from native and invaded habitats
topic biological invasion
ascidian
<i>Ciona intestinalis</i>
Prince Edward Island
microbiome
symbionts
url https://www.mdpi.com/2076-2607/8/12/2022
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