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Title: Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms

Abstract

Dynamic environmental factors such as light, nutrients, salt, and temperature continuously affect chlorophototrophic microbial mats, requiring adaptative and acclimative responses to stabilize composition and function. Quantitative metabolomics analysis can provide insights into metabolite dynamics for understanding community response to such changing environmental conditions. In this study, we quantified volatile organic acids, polar metabolites (amino acids, glycolytic and citric acid cycle intermediates, nucleobases, nucleosides, and sugars), wax esters, and polyhydroxyalkanoates, resulting in the identification of 104 metabolites and related molecules in thermal chlorophototrophic microbial mat cores collected over a diel cycle in Mushroom Spring, Yellowstone National Park. A limited number of predominant taxa inhabiting this community and their functional potentials have been previously identified through metagenomic and metatranscriptomic analyses and in situ metabolisms and metabolic interactions among these taxa have been hypothesized. Our metabolomics results confirmed the diel cycling of photorespiration (e.g. glycolate) and fermentation (e.g. acetate, propionate, and lactate) products, the carbon storage polymers polyhydroxyalkanoates, and dissolved gases (e.g. H2 and CO2) in the waters overlying the mat, which were hypothesized to occur in major mat chlorophototrophic community members. In addition, we have formulated the following new hypotheses: 1) the morning hours are a time of biosynthesis of amino acids,more » DNA, and RNA; 2) Synechococcus spp. produce CH4 via metabolism of phosphonates, and photo-inhibited cells may also produce lactate via fermentation as an alternate metabolism; 3) glycolate and lactate are exchanged among Synechococcus and Roseiflexus spp.; and 4) fluctuations in many metabolite pools (e.g. wax esters) at different times of day result from species found at different depths within the mat responding to temporal differences in their niches.« less

Authors:
; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1182892
Report Number(s):
PNNL-SA-107334
Journal ID: ISSN 1664-302X; 48680; KP1601010
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; Environmental Molecular Sciences Laboratory

Citation Formats

Kim, Young-Mo, Nowack, Shane, Olsen, Millie, Becraft, Eric, Wood, Jason M., Thiel, Vera, Klapper, Isaac, Kuhl, Michael, Fredrickson, Jim K., Bryant, Donald A., Ward, David M., and Metz, Thomas O. Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms. United States: N. p., 2015. Web. doi:10.3389/fmicb.2015.00209.
Kim, Young-Mo, Nowack, Shane, Olsen, Millie, Becraft, Eric, Wood, Jason M., Thiel, Vera, Klapper, Isaac, Kuhl, Michael, Fredrickson, Jim K., Bryant, Donald A., Ward, David M., & Metz, Thomas O. Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms. United States. https://doi.org/10.3389/fmicb.2015.00209
Kim, Young-Mo, Nowack, Shane, Olsen, Millie, Becraft, Eric, Wood, Jason M., Thiel, Vera, Klapper, Isaac, Kuhl, Michael, Fredrickson, Jim K., Bryant, Donald A., Ward, David M., and Metz, Thomas O. Fri . "Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms". United States. https://doi.org/10.3389/fmicb.2015.00209. https://www.osti.gov/servlets/purl/1182892.
@article{osti_1182892,
title = {Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms},
author = {Kim, Young-Mo and Nowack, Shane and Olsen, Millie and Becraft, Eric and Wood, Jason M. and Thiel, Vera and Klapper, Isaac and Kuhl, Michael and Fredrickson, Jim K. and Bryant, Donald A. and Ward, David M. and Metz, Thomas O.},
abstractNote = {Dynamic environmental factors such as light, nutrients, salt, and temperature continuously affect chlorophototrophic microbial mats, requiring adaptative and acclimative responses to stabilize composition and function. Quantitative metabolomics analysis can provide insights into metabolite dynamics for understanding community response to such changing environmental conditions. In this study, we quantified volatile organic acids, polar metabolites (amino acids, glycolytic and citric acid cycle intermediates, nucleobases, nucleosides, and sugars), wax esters, and polyhydroxyalkanoates, resulting in the identification of 104 metabolites and related molecules in thermal chlorophototrophic microbial mat cores collected over a diel cycle in Mushroom Spring, Yellowstone National Park. A limited number of predominant taxa inhabiting this community and their functional potentials have been previously identified through metagenomic and metatranscriptomic analyses and in situ metabolisms and metabolic interactions among these taxa have been hypothesized. Our metabolomics results confirmed the diel cycling of photorespiration (e.g. glycolate) and fermentation (e.g. acetate, propionate, and lactate) products, the carbon storage polymers polyhydroxyalkanoates, and dissolved gases (e.g. H2 and CO2) in the waters overlying the mat, which were hypothesized to occur in major mat chlorophototrophic community members. In addition, we have formulated the following new hypotheses: 1) the morning hours are a time of biosynthesis of amino acids, DNA, and RNA; 2) Synechococcus spp. produce CH4 via metabolism of phosphonates, and photo-inhibited cells may also produce lactate via fermentation as an alternate metabolism; 3) glycolate and lactate are exchanged among Synechococcus and Roseiflexus spp.; and 4) fluctuations in many metabolite pools (e.g. wax esters) at different times of day result from species found at different depths within the mat responding to temporal differences in their niches.},
doi = {10.3389/fmicb.2015.00209},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Fri Apr 17 00:00:00 EDT 2015},
month = {Fri Apr 17 00:00:00 EDT 2015}
}

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Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses
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