Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes

ABSTRACT Microbes are critical in carbon and nutrient cycling in freshwater ecosystems. Members of the Verrucomicrobia are ubiquitous in such systems, and yet their roles and ecophysiology are not well understood. In this study, we recovered 19 Verrucomicrobia draft genomes by sequencing 184 time-se...

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Autores principales:	Shaomei He, Sarah L. R. Stevens, Leong-Keat Chan, Stefan Bertilsson, Tijana Glavina del Rio, Susannah G. Tringe, Rex R. Malmstrom, Katherine D. McMahon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	cytochromes freshwater glycoside hydrolase verrucomicrobia Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2cdceedebb04408e829841a8a27a477a
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spelling	oai:doaj.org-article:2cdceedebb04408e829841a8a27a477a2021-11-15T15:22:05ZEcophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes10.1128/mSphere.00277-172379-5042https://doaj.org/article/2cdceedebb04408e829841a8a27a477a2017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00277-17https://doaj.org/toc/2379-5042ABSTRACT Microbes are critical in carbon and nutrient cycling in freshwater ecosystems. Members of the Verrucomicrobia are ubiquitous in such systems, and yet their roles and ecophysiology are not well understood. In this study, we recovered 19 Verrucomicrobia draft genomes by sequencing 184 time-series metagenomes from a eutrophic lake and a humic bog that differ in carbon source and nutrient availabilities. These genomes span four of the seven previously defined Verrucomicrobia subdivisions and greatly expand knowledge of the genomic diversity of freshwater Verrucomicrobia. Genome analysis revealed their potential role as (poly)saccharide degraders in freshwater, uncovered interesting genomic features for this lifestyle, and suggested their adaptation to nutrient availabilities in their environments. Verrucomicrobia populations differ significantly between the two lakes in glycoside hydrolase gene abundance and functional profiles, reflecting the autochthonous and terrestrially derived allochthonous carbon sources of the two ecosystems, respectively. Interestingly, a number of genomes recovered from the bog contained gene clusters that potentially encode a novel porin-multiheme cytochrome c complex and might be involved in extracellular electron transfer in the anoxic humus-rich environment. Notably, most epilimnion genomes have large numbers of so-called “Planctomycete-specific” cytochrome c-encoding genes, which exhibited distribution patterns nearly opposite to those seen with glycoside hydrolase genes, probably associated with the different levels of environmental oxygen availability and carbohydrate complexity between lakes/layers. Overall, the recovered genomes represent a major step toward understanding the role, ecophysiology, and distribution of Verrucomicrobia in freshwater. IMPORTANCE Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. Here, we greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling.Shaomei HeSarah L. R. StevensLeong-Keat ChanStefan BertilssonTijana Glavina del RioSusannah G. TringeRex R. MalmstromKatherine D. McMahonAmerican Society for Microbiologyarticlecytochromesfreshwaterglycoside hydrolaseverrucomicrobiaMicrobiologyQR1-502ENmSphere, Vol 2, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	cytochromes freshwater glycoside hydrolase verrucomicrobia Microbiology QR1-502
spellingShingle	cytochromes freshwater glycoside hydrolase verrucomicrobia Microbiology QR1-502 Shaomei He Sarah L. R. Stevens Leong-Keat Chan Stefan Bertilsson Tijana Glavina del Rio Susannah G. Tringe Rex R. Malmstrom Katherine D. McMahon Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
description	ABSTRACT Microbes are critical in carbon and nutrient cycling in freshwater ecosystems. Members of the Verrucomicrobia are ubiquitous in such systems, and yet their roles and ecophysiology are not well understood. In this study, we recovered 19 Verrucomicrobia draft genomes by sequencing 184 time-series metagenomes from a eutrophic lake and a humic bog that differ in carbon source and nutrient availabilities. These genomes span four of the seven previously defined Verrucomicrobia subdivisions and greatly expand knowledge of the genomic diversity of freshwater Verrucomicrobia. Genome analysis revealed their potential role as (poly)saccharide degraders in freshwater, uncovered interesting genomic features for this lifestyle, and suggested their adaptation to nutrient availabilities in their environments. Verrucomicrobia populations differ significantly between the two lakes in glycoside hydrolase gene abundance and functional profiles, reflecting the autochthonous and terrestrially derived allochthonous carbon sources of the two ecosystems, respectively. Interestingly, a number of genomes recovered from the bog contained gene clusters that potentially encode a novel porin-multiheme cytochrome c complex and might be involved in extracellular electron transfer in the anoxic humus-rich environment. Notably, most epilimnion genomes have large numbers of so-called “Planctomycete-specific” cytochrome c-encoding genes, which exhibited distribution patterns nearly opposite to those seen with glycoside hydrolase genes, probably associated with the different levels of environmental oxygen availability and carbohydrate complexity between lakes/layers. Overall, the recovered genomes represent a major step toward understanding the role, ecophysiology, and distribution of Verrucomicrobia in freshwater. IMPORTANCE Freshwater Verrucomicrobia spp. are cosmopolitan in lakes and rivers, and yet their roles and ecophysiology are not well understood, as cultured freshwater Verrucomicrobia spp. are restricted to one subdivision of this phylum. Here, we greatly expanded the known genomic diversity of this freshwater lineage by recovering 19 Verrucomicrobia draft genomes from 184 metagenomes collected from a eutrophic lake and a humic bog across multiple years. Most of these genomes represent the first freshwater representatives of several Verrucomicrobia subdivisions. Genomic analysis revealed Verrucomicrobia to be potential (poly)saccharide degraders and suggested their adaptation to carbon sources of different origins in the two contrasting ecosystems. We identified putative extracellular electron transfer genes and so-called “Planctomycete-specific” cytochrome c-encoding genes and identified their distinct distribution patterns between the lakes/layers. Overall, our analysis greatly advances the understanding of the function, ecophysiology, and distribution of freshwater Verrucomicrobia, while highlighting their potential role in freshwater carbon cycling.
format	article
author	Shaomei He Sarah L. R. Stevens Leong-Keat Chan Stefan Bertilsson Tijana Glavina del Rio Susannah G. Tringe Rex R. Malmstrom Katherine D. McMahon
author_facet	Shaomei He Sarah L. R. Stevens Leong-Keat Chan Stefan Bertilsson Tijana Glavina del Rio Susannah G. Tringe Rex R. Malmstrom Katherine D. McMahon
author_sort	Shaomei He
title	Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
title_short	Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
title_full	Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
title_fullStr	Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
title_full_unstemmed	Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes
title_sort	ecophysiology of freshwater verrucomicrobia inferred from metagenome-assembled genomes
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/2cdceedebb04408e829841a8a27a477a
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Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes

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