Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface

ABSTRACT Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Sophie L. Nixon, Rebecca A. Daly, Mikayla A. Borton, Lindsey M. Solden, Susan A. Welch, David R. Cole, Paula J. Mouser, Michael J. Wilkins, Kelly C. Wrighton
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	glycoside hydrolases viruses shale hypersaline hydraulic fracturing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/80c2c7f7ae9b4985ad9439cdffb49c39
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:80c2c7f7ae9b4985ad9439cdffb49c39
record_format	dspace
spelling	oai:doaj.org-article:80c2c7f7ae9b4985ad9439cdffb49c392021-11-15T15:22:24ZGenome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface10.1128/mSphere.00613-192379-5042https://doaj.org/article/80c2c7f7ae9b4985ad9439cdffb49c392019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00613-19https://doaj.org/toc/2379-5042ABSTRACT Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, the Verrucomicrobia are underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of the Verrucomicrobia phylum by describing a novel genus, “Candidatus Marcellius,” belonging to the order Opitutales. “Ca. Marcellius” was recovered from a shale-derived produced fluid metagenome collected 313 days after hydraulic fracturing, the deepest environment from which a member of the Verrucomicrobia has been recovered to date. We uncover genomic attributes that may explain the capacity of this organism to inhabit a shale gas well, including the potential for utilization of organic polymers common in hydraulic fracturing fluids, nitrogen fixation, adaptation to high salinities, and adaptive immunity via CRISPR-Cas. To illuminate the phylogenetic and environmental distribution of these metabolic and adaptive traits across the Verrucomicrobia phylum, we performed a comparative genomic analysis of 31 publicly available, nearly complete Verrucomicrobia genomes. Our genomic findings extend the environmental distribution of the Verrucomicrobia 2.3 kilometers into the terrestrial subsurface. Moreover, we reveal traits widely encoded across members of the Verrucomicrobia, including the capacity to degrade hemicellulose and to adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum. IMPORTANCE The Verrucomicrobia phylum of bacteria is widespread in many different ecosystems; however, its role in microbial communities remains poorly understood. Verrucomicrobia are often low-abundance community members, yet previous research suggests they play a major role in organic carbon degradation. While Verrucomicrobia remain poorly represented in culture collections, numerous genomes have been reconstructed from metagenomic data sets in recent years. The study of genomes from across the phylum allows for an extensive assessment of their potential ecosystem roles. The significance of this work is (i) the recovery of a novel genus of Verrucomicrobia from 2.3 km in the subsurface with the ability to withstand the extreme conditions that characterize this environment, and (ii) the most extensive assessment of ecophysiological traits encoded by Verrucomicrobia genomes to date. We show that members of this phylum are specialist organic polymer degraders that can withstand a wider range of environmental conditions than previously thought.Sophie L. NixonRebecca A. DalyMikayla A. BortonLindsey M. SoldenSusan A. WelchDavid R. ColePaula J. MouserMichael J. WilkinsKelly C. WrightonAmerican Society for Microbiologyarticleglycoside hydrolasesvirusesshalehypersalinehydraulic fracturingMicrobiologyQR1-502ENmSphere, Vol 4, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	glycoside hydrolases viruses shale hypersaline hydraulic fracturing Microbiology QR1-502
spellingShingle	glycoside hydrolases viruses shale hypersaline hydraulic fracturing Microbiology QR1-502 Sophie L. Nixon Rebecca A. Daly Mikayla A. Borton Lindsey M. Solden Susan A. Welch David R. Cole Paula J. Mouser Michael J. Wilkins Kelly C. Wrighton Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface
description	ABSTRACT Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across Earth’s ecosystems. Despite their prevalence, the Verrucomicrobia are underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of the Verrucomicrobia phylum by describing a novel genus, “Candidatus Marcellius,” belonging to the order Opitutales. “Ca. Marcellius” was recovered from a shale-derived produced fluid metagenome collected 313 days after hydraulic fracturing, the deepest environment from which a member of the Verrucomicrobia has been recovered to date. We uncover genomic attributes that may explain the capacity of this organism to inhabit a shale gas well, including the potential for utilization of organic polymers common in hydraulic fracturing fluids, nitrogen fixation, adaptation to high salinities, and adaptive immunity via CRISPR-Cas. To illuminate the phylogenetic and environmental distribution of these metabolic and adaptive traits across the Verrucomicrobia phylum, we performed a comparative genomic analysis of 31 publicly available, nearly complete Verrucomicrobia genomes. Our genomic findings extend the environmental distribution of the Verrucomicrobia 2.3 kilometers into the terrestrial subsurface. Moreover, we reveal traits widely encoded across members of the Verrucomicrobia, including the capacity to degrade hemicellulose and to adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum. IMPORTANCE The Verrucomicrobia phylum of bacteria is widespread in many different ecosystems; however, its role in microbial communities remains poorly understood. Verrucomicrobia are often low-abundance community members, yet previous research suggests they play a major role in organic carbon degradation. While Verrucomicrobia remain poorly represented in culture collections, numerous genomes have been reconstructed from metagenomic data sets in recent years. The study of genomes from across the phylum allows for an extensive assessment of their potential ecosystem roles. The significance of this work is (i) the recovery of a novel genus of Verrucomicrobia from 2.3 km in the subsurface with the ability to withstand the extreme conditions that characterize this environment, and (ii) the most extensive assessment of ecophysiological traits encoded by Verrucomicrobia genomes to date. We show that members of this phylum are specialist organic polymer degraders that can withstand a wider range of environmental conditions than previously thought.
format	article
author	Sophie L. Nixon Rebecca A. Daly Mikayla A. Borton Lindsey M. Solden Susan A. Welch David R. Cole Paula J. Mouser Michael J. Wilkins Kelly C. Wrighton
author_facet	Sophie L. Nixon Rebecca A. Daly Mikayla A. Borton Lindsey M. Solden Susan A. Welch David R. Cole Paula J. Mouser Michael J. Wilkins Kelly C. Wrighton
author_sort	Sophie L. Nixon
title	Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface
title_short	Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface
title_full	Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface
title_fullStr	Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface
title_full_unstemmed	Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface
title_sort	genome-resolved metagenomics extends the environmental distribution of the <italic toggle="yes">verrucomicrobia</italic> phylum to the deep terrestrial subsurface
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/80c2c7f7ae9b4985ad9439cdffb49c39
work_keys_str_mv	AT sophielnixon genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT rebeccaadaly genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT mikaylaaborton genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT lindseymsolden genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT susanawelch genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT davidrcole genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT paulajmouser genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT michaeljwilkins genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface AT kellycwrighton genomeresolvedmetagenomicsextendstheenvironmentaldistributionoftheitalictoggleyesverrucomicrobiaitalicphylumtothedeepterrestrialsubsurface
_version_	1718428016444440576

Genome-Resolved Metagenomics Extends the Environmental Distribution of the <italic toggle="yes">Verrucomicrobia</italic> Phylum to the Deep Terrestrial Subsurface

Ejemplares similares