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

Young Mo Kim, Shane Nowack, Millie Olsen, Eric D. Becraft, Jason M. Wood, Vera Thiel, Isaac Klapper, Michael Kühl, James K. Fredrickson, Donald Ashley Bryant, David M. Ward, Thomas O. Metz

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

Dynamic environmental factors such as light, nutrients, salt, and temperature continuously affect chlorophototrophic microbial mats, requiring adaptive 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 inhabit 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) 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.

Original languageEnglish (US)
Article number209
JournalFrontiers in Microbiology
Volume6
Issue numberMAR
DOIs
StatePublished - Jan 1 2015

Fingerprint

glycolic acid
Hot Springs
Metabolomics
Polyhydroxyalkanoates
Lactic Acid
Waxes
Fermentation
Esters
Synechococcus
Amino Acids
Metagenomics
Citric Acid Cycle
Agaricales
Propionates
Nucleosides
Polymers
Acetates
Carbon
Salts
Hot Temperature

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Microbiology (medical)

Cite this

Kim, Young Mo ; Nowack, Shane ; Olsen, Millie ; Becraft, Eric D. ; Wood, Jason M. ; Thiel, Vera ; Klapper, Isaac ; Kühl, Michael ; Fredrickson, James K. ; Bryant, Donald Ashley ; Ward, David M. ; Metz, Thomas O. / Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms. In: Frontiers in Microbiology. 2015 ; Vol. 6, No. MAR.
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abstract = "Dynamic environmental factors such as light, nutrients, salt, and temperature continuously affect chlorophototrophic microbial mats, requiring adaptive 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 inhabit 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) 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.",
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Kim, YM, Nowack, S, Olsen, M, Becraft, ED, Wood, JM, Thiel, V, Klapper, I, Kühl, M, Fredrickson, JK, Bryant, DA, Ward, DM & Metz, TO 2015, 'Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms', Frontiers in Microbiology, vol. 6, no. MAR, 209. https://doi.org/10.3389/fmicb.2015.00209

Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms. / Kim, Young Mo; Nowack, Shane; Olsen, Millie; Becraft, Eric D.; Wood, Jason M.; Thiel, Vera; Klapper, Isaac; Kühl, Michael; Fredrickson, James K.; Bryant, Donald Ashley; Ward, David M.; Metz, Thomas O.

In: Frontiers in Microbiology, Vol. 6, No. MAR, 209, 01.01.2015.

Research output: Contribution to journalArticle

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T1 - Diel metabolomics analysis of a hot spring chlorophototrophic microbial mat leads to new hypotheses of community member metabolisms

AU - Kim, Young Mo

AU - Nowack, Shane

AU - Olsen, Millie

AU - Becraft, Eric D.

AU - Wood, Jason M.

AU - Thiel, Vera

AU - Klapper, Isaac

AU - Kühl, Michael

AU - Fredrickson, James K.

AU - Bryant, Donald Ashley

AU - Ward, David M.

AU - Metz, Thomas O.

PY - 2015/1/1

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N2 - Dynamic environmental factors such as light, nutrients, salt, and temperature continuously affect chlorophototrophic microbial mats, requiring adaptive 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 inhabit 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) 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.

AB - Dynamic environmental factors such as light, nutrients, salt, and temperature continuously affect chlorophototrophic microbial mats, requiring adaptive 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 inhabit 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) 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.

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