Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution

Abstract Background Fish skin mucosal surfaces (SMS) are quite similar in composition and function to some mammalian MS and, in consequence, could constitute an adequate niche for the evolution of mucosal aquatic pathogens in natural environments. We aimed to test this hypothesis by searching for me...

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Published in:Microbiome
Main Authors: Miguel Carda-Diéguez, Rohit Ghai, Francisco Rodríguez-Valera, Carmen Amaro
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2017
Subjects:
Online Access:https://doi.org/10.1186/s40168-017-0376-1
https://doaj.org/article/e17a2e191a3d47ffb55f0841a4572c0c
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spelling ftdoajarticles:oai:doaj.org/article:e17a2e191a3d47ffb55f0841a4572c0c 2023-05-15T13:28:11+02:00 Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution Miguel Carda-Diéguez Rohit Ghai Francisco Rodríguez-Valera Carmen Amaro 2017-12-01T00:00:00Z https://doi.org/10.1186/s40168-017-0376-1 https://doaj.org/article/e17a2e191a3d47ffb55f0841a4572c0c EN eng BMC http://link.springer.com/article/10.1186/s40168-017-0376-1 https://doaj.org/toc/2049-2618 doi:10.1186/s40168-017-0376-1 2049-2618 https://doaj.org/article/e17a2e191a3d47ffb55f0841a4572c0c Microbiome, Vol 5, Iss 1, Pp 1-15 (2017) Vibrio Skin mucus Microbiome Metagenomics Attached microbiota Microbial ecology QR100-130 article 2017 ftdoajarticles https://doi.org/10.1186/s40168-017-0376-1 2022-12-31T14:14:15Z Abstract Background Fish skin mucosal surfaces (SMS) are quite similar in composition and function to some mammalian MS and, in consequence, could constitute an adequate niche for the evolution of mucosal aquatic pathogens in natural environments. We aimed to test this hypothesis by searching for metagenomic and genomic evidences in the SMS-microbiome of a model fish species (Anguilla Anguilla or eel), from different ecosystems (four natural environments of different water salinity and one eel farm) as well as the water microbiome (W-microbiome) surrounding the host. Results Remarkably, potentially pathogenic Vibrio monopolized wild eel SMS-microbiome from natural ecosystems, Vibrio anguillarum/Vibrio vulnificus and Vibrio cholerae/Vibrio metoecus being the most abundant ones in SMS from estuary and lake, respectively. Functions encoded in the SMS-microbiome differed significantly from those in the W-microbiome and allowed us to predict that successful mucus colonizers should have specific genes for (i) attachment (mainly by forming biofilms), (ii) bacterial competence and communication, and (iii) resistance to mucosal innate immunity, predators (amoeba), and heavy metals/drugs. In addition, we found several mobile genetic elements (mainly integrative conjugative elements) as well as a series of evidences suggesting that bacteria exchange DNA in SMS. Further, we isolated and sequenced a V. metoecus strain from SMS. This isolate shares pathogenicity islands with V. cholerae O1 from intestinal infections that are absent in the rest of sequenced V. metoecus strains, all of them from water and extra-intestinal infections. Conclusions We have obtained metagenomic and genomic evidence in favor of the hypothesis on the role of fish mucosal surfaces as a specialized habitat selecting microbes capable of colonizing and persisting on other comparable mucosal surfaces, e.g., the human intestine. Article in Journal/Newspaper Anguilla anguilla Directory of Open Access Journals: DOAJ Articles Microbiome 5 1
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Vibrio
Skin mucus
Microbiome
Metagenomics
Attached microbiota
Microbial ecology
QR100-130
spellingShingle Vibrio
Skin mucus
Microbiome
Metagenomics
Attached microbiota
Microbial ecology
QR100-130
Miguel Carda-Diéguez
Rohit Ghai
Francisco Rodríguez-Valera
Carmen Amaro
Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution
topic_facet Vibrio
Skin mucus
Microbiome
Metagenomics
Attached microbiota
Microbial ecology
QR100-130
description Abstract Background Fish skin mucosal surfaces (SMS) are quite similar in composition and function to some mammalian MS and, in consequence, could constitute an adequate niche for the evolution of mucosal aquatic pathogens in natural environments. We aimed to test this hypothesis by searching for metagenomic and genomic evidences in the SMS-microbiome of a model fish species (Anguilla Anguilla or eel), from different ecosystems (four natural environments of different water salinity and one eel farm) as well as the water microbiome (W-microbiome) surrounding the host. Results Remarkably, potentially pathogenic Vibrio monopolized wild eel SMS-microbiome from natural ecosystems, Vibrio anguillarum/Vibrio vulnificus and Vibrio cholerae/Vibrio metoecus being the most abundant ones in SMS from estuary and lake, respectively. Functions encoded in the SMS-microbiome differed significantly from those in the W-microbiome and allowed us to predict that successful mucus colonizers should have specific genes for (i) attachment (mainly by forming biofilms), (ii) bacterial competence and communication, and (iii) resistance to mucosal innate immunity, predators (amoeba), and heavy metals/drugs. In addition, we found several mobile genetic elements (mainly integrative conjugative elements) as well as a series of evidences suggesting that bacteria exchange DNA in SMS. Further, we isolated and sequenced a V. metoecus strain from SMS. This isolate shares pathogenicity islands with V. cholerae O1 from intestinal infections that are absent in the rest of sequenced V. metoecus strains, all of them from water and extra-intestinal infections. Conclusions We have obtained metagenomic and genomic evidence in favor of the hypothesis on the role of fish mucosal surfaces as a specialized habitat selecting microbes capable of colonizing and persisting on other comparable mucosal surfaces, e.g., the human intestine.
format Article in Journal/Newspaper
author Miguel Carda-Diéguez
Rohit Ghai
Francisco Rodríguez-Valera
Carmen Amaro
author_facet Miguel Carda-Diéguez
Rohit Ghai
Francisco Rodríguez-Valera
Carmen Amaro
author_sort Miguel Carda-Diéguez
title Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution
title_short Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution
title_full Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution
title_fullStr Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution
title_full_unstemmed Wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution
title_sort wild eel microbiome reveals that skin mucus of fish could be a natural niche for aquatic mucosal pathogen evolution
publisher BMC
publishDate 2017
url https://doi.org/10.1186/s40168-017-0376-1
https://doaj.org/article/e17a2e191a3d47ffb55f0841a4572c0c
genre Anguilla anguilla
genre_facet Anguilla anguilla
op_source Microbiome, Vol 5, Iss 1, Pp 1-15 (2017)
op_relation http://link.springer.com/article/10.1186/s40168-017-0376-1
https://doaj.org/toc/2049-2618
doi:10.1186/s40168-017-0376-1
2049-2618
https://doaj.org/article/e17a2e191a3d47ffb55f0841a4572c0c
op_doi https://doi.org/10.1186/s40168-017-0376-1
container_title Microbiome
container_volume 5
container_issue 1
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