Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>

ABSTRACT The verrucomicrobial subdivision 2 class Spartobacteria is one of the most abundant bacterial lineages in soil and has recently also been found to be ubiquitous in aquatic environments. A 16S rRNA gene study from samples spanning the entire salinity range of the Baltic Sea indicated that, i...

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Autores principales:	Daniel P. R. Herlemann, Daniel Lundin, Matthias Labrenz, Klaus Jürgens, Zongli Zheng, Henrik Aspeborg, Anders F. Andersson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fd6df899170a4daebdd2d537a113c7b1
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spelling	oai:doaj.org-article:fd6df899170a4daebdd2d537a113c7b12021-11-15T15:40:06ZMetagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>10.1128/mBio.00569-122150-7511https://doaj.org/article/fd6df899170a4daebdd2d537a113c7b12013-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00569-12https://doaj.org/toc/2150-7511ABSTRACT The verrucomicrobial subdivision 2 class Spartobacteria is one of the most abundant bacterial lineages in soil and has recently also been found to be ubiquitous in aquatic environments. A 16S rRNA gene study from samples spanning the entire salinity range of the Baltic Sea indicated that, in the pelagic brackish water, a phylotype of the Spartobacteria is one of the dominating bacteria during summer. Phylogenetic analyses of related 16S rRNA genes indicate that a purely aquatic lineage within the Spartobacteria exists. Since no aquatic representative from the Spartobacteria has been cultured or sequenced, the metabolic capacity and ecological role of this lineage are yet unknown. In this study, we reconstructed the genome and metabolic potential of the abundant Baltic Sea Spartobacteria phylotype by metagenomics. Binning of genome fragments by nucleotide composition and a self-organizing map recovered the near-complete genome of the organism, the gene content of which suggests an aerobic heterotrophic metabolism. Notably, we found 23 glycoside hydrolases that likely allow the use of a variety of carbohydrates, like cellulose, mannan, xylan, chitin, and starch, as carbon sources. In addition, a complete pathway for sulfate utilization was found, indicating catabolic processing of sulfated polysaccharides, commonly found in aquatic phytoplankton. The high frequency of glycoside hydrolase genes implies an important role of this organism in the aquatic carbon cycle. Spatiotemporal data of the phylotype’s distribution within the Baltic Sea indicate a connection to Cyanobacteria that may be the main source of the polysaccharide substrates. IMPORTANCE The ecosystem roles of many phylogenetic lineages are not yet well understood. One such lineage is the class Spartobacteria within the Verrucomicrobia that, despite being abundant in soil and aquatic systems, is relatively poorly studied. Here we circumvented the difficulties of growing aquatic Verrucomicrobia by applying shotgun metagenomic sequencing on a water sample from the Baltic Sea. By using a method based on sequence signatures, we were able to in silico isolate genome fragments belonging to a phylotype of the Spartobacteria. The genome, which represents the first aquatic representative of this clade, encodes a diversity of glycoside hydrolases that likely allow degradation of various complex carbohydrates. Since the phylotype cooccurs with Cyanobacteria, these may be the primary producers of the carbohydrate substrates. The phylotype, which is highly abundant in the Baltic Sea during summer, may thus play an important role in the carbon cycle of this ecosystem.Daniel P. R. HerlemannDaniel LundinMatthias LabrenzKlaus JürgensZongli ZhengHenrik AspeborgAnders F. AnderssonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 3 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Daniel P. R. Herlemann Daniel Lundin Matthias Labrenz Klaus Jürgens Zongli Zheng Henrik Aspeborg Anders F. Andersson Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>
description	ABSTRACT The verrucomicrobial subdivision 2 class Spartobacteria is one of the most abundant bacterial lineages in soil and has recently also been found to be ubiquitous in aquatic environments. A 16S rRNA gene study from samples spanning the entire salinity range of the Baltic Sea indicated that, in the pelagic brackish water, a phylotype of the Spartobacteria is one of the dominating bacteria during summer. Phylogenetic analyses of related 16S rRNA genes indicate that a purely aquatic lineage within the Spartobacteria exists. Since no aquatic representative from the Spartobacteria has been cultured or sequenced, the metabolic capacity and ecological role of this lineage are yet unknown. In this study, we reconstructed the genome and metabolic potential of the abundant Baltic Sea Spartobacteria phylotype by metagenomics. Binning of genome fragments by nucleotide composition and a self-organizing map recovered the near-complete genome of the organism, the gene content of which suggests an aerobic heterotrophic metabolism. Notably, we found 23 glycoside hydrolases that likely allow the use of a variety of carbohydrates, like cellulose, mannan, xylan, chitin, and starch, as carbon sources. In addition, a complete pathway for sulfate utilization was found, indicating catabolic processing of sulfated polysaccharides, commonly found in aquatic phytoplankton. The high frequency of glycoside hydrolase genes implies an important role of this organism in the aquatic carbon cycle. Spatiotemporal data of the phylotype’s distribution within the Baltic Sea indicate a connection to Cyanobacteria that may be the main source of the polysaccharide substrates. IMPORTANCE The ecosystem roles of many phylogenetic lineages are not yet well understood. One such lineage is the class Spartobacteria within the Verrucomicrobia that, despite being abundant in soil and aquatic systems, is relatively poorly studied. Here we circumvented the difficulties of growing aquatic Verrucomicrobia by applying shotgun metagenomic sequencing on a water sample from the Baltic Sea. By using a method based on sequence signatures, we were able to in silico isolate genome fragments belonging to a phylotype of the Spartobacteria. The genome, which represents the first aquatic representative of this clade, encodes a diversity of glycoside hydrolases that likely allow degradation of various complex carbohydrates. Since the phylotype cooccurs with Cyanobacteria, these may be the primary producers of the carbohydrate substrates. The phylotype, which is highly abundant in the Baltic Sea during summer, may thus play an important role in the carbon cycle of this ecosystem.
format	article
author	Daniel P. R. Herlemann Daniel Lundin Matthias Labrenz Klaus Jürgens Zongli Zheng Henrik Aspeborg Anders F. Andersson
author_facet	Daniel P. R. Herlemann Daniel Lundin Matthias Labrenz Klaus Jürgens Zongli Zheng Henrik Aspeborg Anders F. Andersson
author_sort	Daniel P. R. Herlemann
title	Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>
title_short	Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>
title_full	Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>
title_fullStr	Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>
title_full_unstemmed	Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>
title_sort	metagenomic <italic toggle="yes">de novo</italic> assembly of an aquatic representative of the verrucomicrobial class <italic toggle="yes">spartobacteria</italic>
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/fd6df899170a4daebdd2d537a113c7b1
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Metagenomic <italic toggle="yes">De Novo</italic> Assembly of an Aquatic Representative of the Verrucomicrobial Class <italic toggle="yes">Spartobacteria</italic>

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