Genomic and metagenomic insights into the microbial community of a thermal spring

Abstract Background Water springs provide important ecosystem services including drinking water supply, recreation, and balneotherapy, but their microbial communities remain largely unknown. In this study, we characterized the spring water microbiome of Comano Terme (Italy) at four sampling points o...

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Main Authors: Renato Pedron, Alfonso Esposito, Irene Bianconi, Edoardo Pasolli, Adrian Tett, Francesco Asnicar, Mario Cristofolini, Nicola Segata, Olivier Jousson
Format: Article
Language:English
Published: BMC 2019-01-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-019-0625-6
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spelling doaj-74819387111e4bbca1f6e9d6e5f4f6202020-11-24T21:40:55ZengBMCMicrobiome2049-26182019-01-017111310.1186/s40168-019-0625-6Genomic and metagenomic insights into the microbial community of a thermal springRenato Pedron0Alfonso Esposito1Irene Bianconi2Edoardo Pasolli3Adrian Tett4Francesco Asnicar5Mario Cristofolini6Nicola Segata7Olivier Jousson8Centre for Integrative Biology, University of TrentoCentre for Integrative Biology, University of TrentoCentre for Integrative Biology, University of TrentoCentre for Integrative Biology, University of TrentoCentre for Integrative Biology, University of TrentoCentre for Integrative Biology, University of TrentoIstituto G.B. MatteiCentre for Integrative Biology, University of TrentoCentre for Integrative Biology, University of TrentoAbstract Background Water springs provide important ecosystem services including drinking water supply, recreation, and balneotherapy, but their microbial communities remain largely unknown. In this study, we characterized the spring water microbiome of Comano Terme (Italy) at four sampling points of the thermal spa, including natural (spring and well) and human-built (storage tank, bathtubs) environments. We integrated large-scale culturing and metagenomic approaches, with the aim of comprehensively determining the spring water taxonomic composition and functional potential. Results The groundwater feeding the spring hosted the most atypical microbiome, including many taxa known to be recalcitrant to cultivation. The core microbiome included the orders Sphingomonadales, Rhizobiales, and Caulobacterales, and the families Bradyrhizobiaceae and Moraxellaceae. A comparative genomic analysis of 72 isolates and 30 metagenome-assembled genomes (MAGs) revealed that most isolates and MAGs belonged to new species or higher taxonomic ranks widely distributed in the microbial tree of life. Average nucleotide identity (ANI) values calculated for each isolated or assembled genome showed that 10 genomes belonged to known bacterial species (> 95% ANI), 36 genomes (including 1 MAG) had ANI values ranging 85–92.5% and could be assigned as undescribed species belonging to known genera, while the remaining 55 genomes had lower ANI values (< 85%). A number of functional features were significantly over- or underrepresented in genomes derived from the four sampling sites. Functional specialization was found between sites, with for example methanogenesis being unique to groundwater whereas methanotrophy was found in all samples. Conclusions Current knowledge on aquatic microbiomes is essentially based on surface or human-associated environments. We started uncovering the spring water microbiome, highlighting an unexpected diversity that should be further investigated. This study confirms that groundwater environments host highly adapted, stable microbial communities composed of many unknown taxa, even among the culturable fraction.http://link.springer.com/article/10.1186/s40168-019-0625-6Shotgun metagenomicsHigh-throughput culturingThermal springComparative genomics
collection DOAJ
language English
format Article
sources DOAJ
author Renato Pedron
Alfonso Esposito
Irene Bianconi
Edoardo Pasolli
Adrian Tett
Francesco Asnicar
Mario Cristofolini
Nicola Segata
Olivier Jousson
spellingShingle Renato Pedron
Alfonso Esposito
Irene Bianconi
Edoardo Pasolli
Adrian Tett
Francesco Asnicar
Mario Cristofolini
Nicola Segata
Olivier Jousson
Genomic and metagenomic insights into the microbial community of a thermal spring
Microbiome
Shotgun metagenomics
High-throughput culturing
Thermal spring
Comparative genomics
author_facet Renato Pedron
Alfonso Esposito
Irene Bianconi
Edoardo Pasolli
Adrian Tett
Francesco Asnicar
Mario Cristofolini
Nicola Segata
Olivier Jousson
author_sort Renato Pedron
title Genomic and metagenomic insights into the microbial community of a thermal spring
title_short Genomic and metagenomic insights into the microbial community of a thermal spring
title_full Genomic and metagenomic insights into the microbial community of a thermal spring
title_fullStr Genomic and metagenomic insights into the microbial community of a thermal spring
title_full_unstemmed Genomic and metagenomic insights into the microbial community of a thermal spring
title_sort genomic and metagenomic insights into the microbial community of a thermal spring
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2019-01-01
description Abstract Background Water springs provide important ecosystem services including drinking water supply, recreation, and balneotherapy, but their microbial communities remain largely unknown. In this study, we characterized the spring water microbiome of Comano Terme (Italy) at four sampling points of the thermal spa, including natural (spring and well) and human-built (storage tank, bathtubs) environments. We integrated large-scale culturing and metagenomic approaches, with the aim of comprehensively determining the spring water taxonomic composition and functional potential. Results The groundwater feeding the spring hosted the most atypical microbiome, including many taxa known to be recalcitrant to cultivation. The core microbiome included the orders Sphingomonadales, Rhizobiales, and Caulobacterales, and the families Bradyrhizobiaceae and Moraxellaceae. A comparative genomic analysis of 72 isolates and 30 metagenome-assembled genomes (MAGs) revealed that most isolates and MAGs belonged to new species or higher taxonomic ranks widely distributed in the microbial tree of life. Average nucleotide identity (ANI) values calculated for each isolated or assembled genome showed that 10 genomes belonged to known bacterial species (> 95% ANI), 36 genomes (including 1 MAG) had ANI values ranging 85–92.5% and could be assigned as undescribed species belonging to known genera, while the remaining 55 genomes had lower ANI values (< 85%). A number of functional features were significantly over- or underrepresented in genomes derived from the four sampling sites. Functional specialization was found between sites, with for example methanogenesis being unique to groundwater whereas methanotrophy was found in all samples. Conclusions Current knowledge on aquatic microbiomes is essentially based on surface or human-associated environments. We started uncovering the spring water microbiome, highlighting an unexpected diversity that should be further investigated. This study confirms that groundwater environments host highly adapted, stable microbial communities composed of many unknown taxa, even among the culturable fraction.
topic Shotgun metagenomics
High-throughput culturing
Thermal spring
Comparative genomics
url http://link.springer.com/article/10.1186/s40168-019-0625-6
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