Position-specific metabolic probing and metagenomics of microbial communities reveal conserved central carbon metabolic network activities at high temperatures

Scott C. Thomas, Kevin O. Tamadonfar, Cale O. Seymour, Dengxun Lai, Jeremy A. Dodsworth, Senthil K. Murugapiran, Emiley A. Eloe-Fadrosh, Paul Dijkstra, Brian P. Hedlund

Research output: Contribution to journalArticle

Abstract

Temperature is a primary driver of microbial community composition and taxonomic diversity; however, it is unclear to what extent temperature affects characteristics of central carbon metabolic pathways (CCMPs) at the community level. In this study, 16S rRNA gene amplicon and metagenome sequencing were combined with 13C-labeled metabolite probing of the CCMPs to assess community carbon metabolism along a temperature gradient (60-95°C) in Great Boiling Spring, NV. 16S rRNA gene amplicon diversity was inversely proportional to temperature, and Archaea were dominant at higher temperatures. KO richness and diversity were also inversely proportional to temperature, yet CCMP genes were similarly represented across the temperature gradient and many individual metagenome-assembled genomes had complete pathways. In contrast, genes encoding cellulosomes and many genes involved in plant matter degradation and photosynthesis were absent at higher temperatures. In situ 13C-CO2 production from labeled isotopomer pairs of glucose, pyruvate, and acetate suggested lower relative oxidative pentose phosphate pathway activity and/or fermentation at 60°C, and a stable or decreased maintenance energy demand at higher temperatures. Catabolism of 13C-labeled citrate, succinate, L-alanine, L-serine, and L-cysteine was observed at 85°C, demonstrating broad heterotrophic activity and confirming functioning of the TCA cycle. Together, these results suggest that temperature-driven losses in biodiversity and gene content in geothermal systems may not alter CCMP function or maintenance energy demands at a community level.

Original languageEnglish (US)
Article number1427
JournalFrontiers in Microbiology
Volume10
Issue numberJULY
DOIs
StatePublished - Jan 1 2019

Fingerprint

Metagenomics
Metabolic Networks and Pathways
Carbon
Temperature
Metagenome
rRNA Genes
Genes
Cellulosomes
Maintenance
Pentose Phosphate Pathway
Biodiversity
Archaea
Photosynthesis
Succinic Acid
Pyruvic Acid
Citric Acid
Alanine
Serine
Fermentation
Cysteine

Keywords

  • C stable isotope
  • Anabolic
  • Catabolic
  • Diversity
  • Heterotrophy
  • Hyperthermophile
  • Isotopomers
  • Thermophile

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

Cite this

Position-specific metabolic probing and metagenomics of microbial communities reveal conserved central carbon metabolic network activities at high temperatures. / Thomas, Scott C.; Tamadonfar, Kevin O.; Seymour, Cale O.; Lai, Dengxun; Dodsworth, Jeremy A.; Murugapiran, Senthil K.; Eloe-Fadrosh, Emiley A.; Dijkstra, Paul; Hedlund, Brian P.

In: Frontiers in Microbiology, Vol. 10, No. JULY, 1427, 01.01.2019.

Research output: Contribution to journalArticle

Thomas, Scott C. ; Tamadonfar, Kevin O. ; Seymour, Cale O. ; Lai, Dengxun ; Dodsworth, Jeremy A. ; Murugapiran, Senthil K. ; Eloe-Fadrosh, Emiley A. ; Dijkstra, Paul ; Hedlund, Brian P. / Position-specific metabolic probing and metagenomics of microbial communities reveal conserved central carbon metabolic network activities at high temperatures. In: Frontiers in Microbiology. 2019 ; Vol. 10, No. JULY.
@article{4e931f5e0e364d18b3f3de69dc432670,
title = "Position-specific metabolic probing and metagenomics of microbial communities reveal conserved central carbon metabolic network activities at high temperatures",
abstract = "Temperature is a primary driver of microbial community composition and taxonomic diversity; however, it is unclear to what extent temperature affects characteristics of central carbon metabolic pathways (CCMPs) at the community level. In this study, 16S rRNA gene amplicon and metagenome sequencing were combined with 13C-labeled metabolite probing of the CCMPs to assess community carbon metabolism along a temperature gradient (60-95°C) in Great Boiling Spring, NV. 16S rRNA gene amplicon diversity was inversely proportional to temperature, and Archaea were dominant at higher temperatures. KO richness and diversity were also inversely proportional to temperature, yet CCMP genes were similarly represented across the temperature gradient and many individual metagenome-assembled genomes had complete pathways. In contrast, genes encoding cellulosomes and many genes involved in plant matter degradation and photosynthesis were absent at higher temperatures. In situ 13C-CO2 production from labeled isotopomer pairs of glucose, pyruvate, and acetate suggested lower relative oxidative pentose phosphate pathway activity and/or fermentation at 60°C, and a stable or decreased maintenance energy demand at higher temperatures. Catabolism of 13C-labeled citrate, succinate, L-alanine, L-serine, and L-cysteine was observed at 85°C, demonstrating broad heterotrophic activity and confirming functioning of the TCA cycle. Together, these results suggest that temperature-driven losses in biodiversity and gene content in geothermal systems may not alter CCMP function or maintenance energy demands at a community level.",
keywords = "C stable isotope, Anabolic, Catabolic, Diversity, Heterotrophy, Hyperthermophile, Isotopomers, Thermophile",
author = "Thomas, {Scott C.} and Tamadonfar, {Kevin O.} and Seymour, {Cale O.} and Dengxun Lai and Dodsworth, {Jeremy A.} and Murugapiran, {Senthil K.} and Eloe-Fadrosh, {Emiley A.} and Paul Dijkstra and Hedlund, {Brian P.}",
year = "2019",
month = "1",
day = "1",
doi = "10.3389/fmicb.2019.01427",
language = "English (US)",
volume = "10",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers Media S. A.",
number = "JULY",

}

TY - JOUR

T1 - Position-specific metabolic probing and metagenomics of microbial communities reveal conserved central carbon metabolic network activities at high temperatures

AU - Thomas, Scott C.

AU - Tamadonfar, Kevin O.

AU - Seymour, Cale O.

AU - Lai, Dengxun

AU - Dodsworth, Jeremy A.

AU - Murugapiran, Senthil K.

AU - Eloe-Fadrosh, Emiley A.

AU - Dijkstra, Paul

AU - Hedlund, Brian P.

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Temperature is a primary driver of microbial community composition and taxonomic diversity; however, it is unclear to what extent temperature affects characteristics of central carbon metabolic pathways (CCMPs) at the community level. In this study, 16S rRNA gene amplicon and metagenome sequencing were combined with 13C-labeled metabolite probing of the CCMPs to assess community carbon metabolism along a temperature gradient (60-95°C) in Great Boiling Spring, NV. 16S rRNA gene amplicon diversity was inversely proportional to temperature, and Archaea were dominant at higher temperatures. KO richness and diversity were also inversely proportional to temperature, yet CCMP genes were similarly represented across the temperature gradient and many individual metagenome-assembled genomes had complete pathways. In contrast, genes encoding cellulosomes and many genes involved in plant matter degradation and photosynthesis were absent at higher temperatures. In situ 13C-CO2 production from labeled isotopomer pairs of glucose, pyruvate, and acetate suggested lower relative oxidative pentose phosphate pathway activity and/or fermentation at 60°C, and a stable or decreased maintenance energy demand at higher temperatures. Catabolism of 13C-labeled citrate, succinate, L-alanine, L-serine, and L-cysteine was observed at 85°C, demonstrating broad heterotrophic activity and confirming functioning of the TCA cycle. Together, these results suggest that temperature-driven losses in biodiversity and gene content in geothermal systems may not alter CCMP function or maintenance energy demands at a community level.

AB - Temperature is a primary driver of microbial community composition and taxonomic diversity; however, it is unclear to what extent temperature affects characteristics of central carbon metabolic pathways (CCMPs) at the community level. In this study, 16S rRNA gene amplicon and metagenome sequencing were combined with 13C-labeled metabolite probing of the CCMPs to assess community carbon metabolism along a temperature gradient (60-95°C) in Great Boiling Spring, NV. 16S rRNA gene amplicon diversity was inversely proportional to temperature, and Archaea were dominant at higher temperatures. KO richness and diversity were also inversely proportional to temperature, yet CCMP genes were similarly represented across the temperature gradient and many individual metagenome-assembled genomes had complete pathways. In contrast, genes encoding cellulosomes and many genes involved in plant matter degradation and photosynthesis were absent at higher temperatures. In situ 13C-CO2 production from labeled isotopomer pairs of glucose, pyruvate, and acetate suggested lower relative oxidative pentose phosphate pathway activity and/or fermentation at 60°C, and a stable or decreased maintenance energy demand at higher temperatures. Catabolism of 13C-labeled citrate, succinate, L-alanine, L-serine, and L-cysteine was observed at 85°C, demonstrating broad heterotrophic activity and confirming functioning of the TCA cycle. Together, these results suggest that temperature-driven losses in biodiversity and gene content in geothermal systems may not alter CCMP function or maintenance energy demands at a community level.

KW - C stable isotope

KW - Anabolic

KW - Catabolic

KW - Diversity

KW - Heterotrophy

KW - Hyperthermophile

KW - Isotopomers

KW - Thermophile

UR - http://www.scopus.com/inward/record.url?scp=85069511112&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85069511112&partnerID=8YFLogxK

U2 - 10.3389/fmicb.2019.01427

DO - 10.3389/fmicb.2019.01427

M3 - Article

AN - SCOPUS:85069511112

VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

IS - JULY

M1 - 1427

ER -