Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces

The advent of culture independent approaches has greatly facilitated insights into the vast diversity of bacteria and the ecological importance they hold in nature and human health. Recently, metagenomic surveys and other culture-independent methods have begun to describe the distribution and divers...

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Main Authors: Marc G. Chevrette, Camila Carlos-Shanley, Katherine B. Louie, Benjamin P. Bowen, Trent R. Northen, Cameron R. Currie
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Microbiology
Subjects:
16S
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02170/full
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spelling doaj-455713f8ef164b98915074059a5cff052020-11-25T02:11:05ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-09-011010.3389/fmicb.2019.02170483731Taxonomic and Metabolic Incongruence in the Ancient Genus StreptomycesMarc G. Chevrette0Camila Carlos-Shanley1Katherine B. Louie2Benjamin P. Bowen3Trent R. Northen4Cameron R. Currie5Department of Plant Pathology, Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Biology, Texas State University, San Marcos, TX, United StatesEnvironmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Joint Genome Institute, Berkeley, CA, United StatesEnvironmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Joint Genome Institute, Berkeley, CA, United StatesEnvironmental Genomics and Systems Biology, Lawrence Berkeley National Laboratory, Joint Genome Institute, Berkeley, CA, United StatesDepartment of Bacteriology, University of Wisconsin-Madison, Madison, WI, United StatesThe advent of culture independent approaches has greatly facilitated insights into the vast diversity of bacteria and the ecological importance they hold in nature and human health. Recently, metagenomic surveys and other culture-independent methods have begun to describe the distribution and diversity of microbial metabolism across environmental conditions, often using 16S rRNA gene as a marker to group bacteria into taxonomic units. However, the extent to which similarity at the conserved ribosomal 16S gene correlates with different measures of phylogeny, metabolic diversity, and ecologically relevant gene content remains contentious. Here, we examine the relationship between 16S identity, core genome divergence, and metabolic gene content across the ancient and ecologically important genus Streptomyces. We assessed and quantified the high variability of average nucleotide identity (ANI) and ortholog presence/absence within Streptomyces, even in strains identical by 16S. Furthermore, we identified key differences in shared ecologically important characters, such as antibiotic resistance, carbohydrate metabolism, biosynthetic gene clusters (BGCs), and other metabolic hallmarks, within 16S identities commonly treated as the same operational taxonomic units (OTUs). Differences between common phylogenetic measures and metabolite-gene annotations confirmed this incongruence. Our results highlight the metabolic diversity and variability within OTUs and add to the growing body of work suggesting 16S-based studies of Streptomyces fail to resolve important ecological and metabolic characteristics.https://www.frontiersin.org/article/10.3389/fmicb.2019.02170/fullStreptomycesmetabolism16Sphylogenomicsmetabolites
collection DOAJ
language English
format Article
sources DOAJ
author Marc G. Chevrette
Camila Carlos-Shanley
Katherine B. Louie
Benjamin P. Bowen
Trent R. Northen
Cameron R. Currie
spellingShingle Marc G. Chevrette
Camila Carlos-Shanley
Katherine B. Louie
Benjamin P. Bowen
Trent R. Northen
Cameron R. Currie
Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces
Frontiers in Microbiology
Streptomyces
metabolism
16S
phylogenomics
metabolites
author_facet Marc G. Chevrette
Camila Carlos-Shanley
Katherine B. Louie
Benjamin P. Bowen
Trent R. Northen
Cameron R. Currie
author_sort Marc G. Chevrette
title Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces
title_short Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces
title_full Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces
title_fullStr Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces
title_full_unstemmed Taxonomic and Metabolic Incongruence in the Ancient Genus Streptomyces
title_sort taxonomic and metabolic incongruence in the ancient genus streptomyces
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-09-01
description The advent of culture independent approaches has greatly facilitated insights into the vast diversity of bacteria and the ecological importance they hold in nature and human health. Recently, metagenomic surveys and other culture-independent methods have begun to describe the distribution and diversity of microbial metabolism across environmental conditions, often using 16S rRNA gene as a marker to group bacteria into taxonomic units. However, the extent to which similarity at the conserved ribosomal 16S gene correlates with different measures of phylogeny, metabolic diversity, and ecologically relevant gene content remains contentious. Here, we examine the relationship between 16S identity, core genome divergence, and metabolic gene content across the ancient and ecologically important genus Streptomyces. We assessed and quantified the high variability of average nucleotide identity (ANI) and ortholog presence/absence within Streptomyces, even in strains identical by 16S. Furthermore, we identified key differences in shared ecologically important characters, such as antibiotic resistance, carbohydrate metabolism, biosynthetic gene clusters (BGCs), and other metabolic hallmarks, within 16S identities commonly treated as the same operational taxonomic units (OTUs). Differences between common phylogenetic measures and metabolite-gene annotations confirmed this incongruence. Our results highlight the metabolic diversity and variability within OTUs and add to the growing body of work suggesting 16S-based studies of Streptomyces fail to resolve important ecological and metabolic characteristics.
topic Streptomyces
metabolism
16S
phylogenomics
metabolites
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02170/full
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