Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics

ABSTRACT Microorganisms grow under a remarkable range of extreme conditions. Environmental transcriptomic and proteomic studies have highlighted metabolic pathways active in extremophilic communities. However, metabolites directly linked to their physiology are less well defined because metabolomics...

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Autores principales:	Annika C. Mosier, Nicholas B. Justice, Benjamin P. Bowen, Richard Baran, Brian C. Thomas, Trent R. Northen, Jillian F. Banfield
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ef3a917bc1b04c7280a1d8c3eb158a08
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spelling	oai:doaj.org-article:ef3a917bc1b04c7280a1d8c3eb158a082021-11-15T15:40:28ZMetabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics10.1128/mBio.00484-122150-7511https://doaj.org/article/ef3a917bc1b04c7280a1d8c3eb158a082013-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00484-12https://doaj.org/toc/2150-7511ABSTRACT Microorganisms grow under a remarkable range of extreme conditions. Environmental transcriptomic and proteomic studies have highlighted metabolic pathways active in extremophilic communities. However, metabolites directly linked to their physiology are less well defined because metabolomics methods lag behind other omics technologies due to a wide range of experimental complexities often associated with the environmental matrix. We identified key metabolites associated with acidophilic and metal-tolerant microorganisms using stable isotope labeling coupled with untargeted, high-resolution mass spectrometry. We observed >3,500 metabolic features in biofilms growing in pH ~0.9 acid mine drainage solutions containing millimolar concentrations of iron, sulfate, zinc, copper, and arsenic. Stable isotope labeling improved chemical formula prediction by >50% for larger metabolites (>250 atomic mass units), many of which were unrepresented in metabolic databases and may represent novel compounds. Taurine and hydroxyectoine were identified and likely provide protection from osmotic stress in the biofilms. Community genomic, transcriptomic, and proteomic data implicate fungi in taurine metabolism. Leptospirillum group II bacteria decrease production of ectoine and hydroxyectoine as biofilms mature, suggesting that biofilm structure provides some resistance to high metal and proton concentrations. The combination of taurine, ectoine, and hydroxyectoine may also constitute a sulfur, nitrogen, and carbon currency in the communities. IMPORTANCE Microbial communities are central to many critical global processes and yet remain enigmatic largely due to their complex and distributed metabolic interactions. Metabolomics has the possibility of providing mechanistic insights into the function and ecology of microbial communities. However, our limited knowledge of microbial metabolites, the difficulty of identifying metabolites from complex samples, and the inability to link metabolites directly to community members have proven to be major limitations in developing advances in systems interactions. Here, we show that combining stable-isotope-enabled metabolomics with genomics, transcriptomics, and proteomics can illuminate the ecology of microorganisms at the community scale.Annika C. MosierNicholas B. JusticeBenjamin P. BowenRichard BaranBrian C. ThomasTrent R. NorthenJillian F. BanfieldAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 2 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Annika C. Mosier Nicholas B. Justice Benjamin P. Bowen Richard Baran Brian C. Thomas Trent R. Northen Jillian F. Banfield Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics
description	ABSTRACT Microorganisms grow under a remarkable range of extreme conditions. Environmental transcriptomic and proteomic studies have highlighted metabolic pathways active in extremophilic communities. However, metabolites directly linked to their physiology are less well defined because metabolomics methods lag behind other omics technologies due to a wide range of experimental complexities often associated with the environmental matrix. We identified key metabolites associated with acidophilic and metal-tolerant microorganisms using stable isotope labeling coupled with untargeted, high-resolution mass spectrometry. We observed >3,500 metabolic features in biofilms growing in pH ~0.9 acid mine drainage solutions containing millimolar concentrations of iron, sulfate, zinc, copper, and arsenic. Stable isotope labeling improved chemical formula prediction by >50% for larger metabolites (>250 atomic mass units), many of which were unrepresented in metabolic databases and may represent novel compounds. Taurine and hydroxyectoine were identified and likely provide protection from osmotic stress in the biofilms. Community genomic, transcriptomic, and proteomic data implicate fungi in taurine metabolism. Leptospirillum group II bacteria decrease production of ectoine and hydroxyectoine as biofilms mature, suggesting that biofilm structure provides some resistance to high metal and proton concentrations. The combination of taurine, ectoine, and hydroxyectoine may also constitute a sulfur, nitrogen, and carbon currency in the communities. IMPORTANCE Microbial communities are central to many critical global processes and yet remain enigmatic largely due to their complex and distributed metabolic interactions. Metabolomics has the possibility of providing mechanistic insights into the function and ecology of microbial communities. However, our limited knowledge of microbial metabolites, the difficulty of identifying metabolites from complex samples, and the inability to link metabolites directly to community members have proven to be major limitations in developing advances in systems interactions. Here, we show that combining stable-isotope-enabled metabolomics with genomics, transcriptomics, and proteomics can illuminate the ecology of microorganisms at the community scale.
format	article
author	Annika C. Mosier Nicholas B. Justice Benjamin P. Bowen Richard Baran Brian C. Thomas Trent R. Northen Jillian F. Banfield
author_facet	Annika C. Mosier Nicholas B. Justice Benjamin P. Bowen Richard Baran Brian C. Thomas Trent R. Northen Jillian F. Banfield
author_sort	Annika C. Mosier
title	Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics
title_short	Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics
title_full	Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics
title_fullStr	Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics
title_full_unstemmed	Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics
title_sort	metabolites associated with adaptation of microorganisms to an acidophilic, metal-rich environment identified by stable-isotope-enabled metabolomics
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/ef3a917bc1b04c7280a1d8c3eb158a08
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Metabolites Associated with Adaptation of Microorganisms to an Acidophilic, Metal-Rich Environment Identified by Stable-Isotope-Enabled Metabolomics

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