Effect of temperature on metabolic activity of intact microbial communities

Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency

Paul Dijkstra, Scott C. Thomas, Paul L. Heinrich, George W Koch, Egbert Schwartz, Bruce A Hungate

Research output: Contribution to journalArticle

93 Citations (Scopus)

Abstract

We used metabolic tracers and modeling to analyze the response of soil metabolism to a sudden change in temperature from 4 to 20 °C. We hypothesized that intact soil microbial communities would exhibit shifts in pentose phosphate pathway and glycolysis activity in the same way as is regularly observed for individual microorganisms in pure culture. We also hypothesized that increased maintenance respiration at higher temperature would result in greater energy production and reduced carbon use efficiency (CUE). Two hours after temperature increase, respiration increased almost 10-fold. Although all metabolic processes were increased, the relative activity of metabolic processes, biosynthesis, and energy production changed. Pentose phosphate pathway was reduced (17-20%), while activities of specific steps in glycolysis (51%) and Krebs cycle (7-13%) were increased. In contrast, only small but significant changes in biosynthesis (+2%), ATP production (-3%) and CUE (+2%) were observed. In a second experiment, we compared the metabolic responses to temperature increases in soils from high and low elevation. The shift in activity from pentose phosphate pathway to glycolysis with higher temperature was confirmed in both soils, but the responses of Krebs cycle, biosynthesis, ATP production, and CUE were site dependent. Our results indicate that 1) in response to temperature, communities behave biochemically similarly to single species and, 2) our understanding of temperature effects on CUE, energy production and use for maintenance and growth processes is still incomplete.

Original languageEnglish (US)
Pages (from-to)2023-2031
Number of pages9
JournalSoil Biology and Biochemistry
Volume43
Issue number10
DOIs
StatePublished - Oct 2011

Fingerprint

Metabolic Networks and Pathways
microbial communities
biochemical pathways
microbial community
Respiration
respiration
Carbon
Maintenance
Temperature
carbon
phosphate
Pentose Phosphate Pathway
pentoses
glycolysis
Glycolysis
Soil
temperature
soil
Citric Acid Cycle
tricarboxylic acid cycle

Keywords

  • C metabolism
  • Carbon
  • Glycolysis
  • Krebs cycle
  • Modeling
  • Pentose phosphate pathway
  • Soil microbial biomass
  • Stable isotopes
  • Temperature

ASJC Scopus subject areas

  • Soil Science
  • Microbiology

Cite this

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title = "Effect of temperature on metabolic activity of intact microbial communities: Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency",
abstract = "We used metabolic tracers and modeling to analyze the response of soil metabolism to a sudden change in temperature from 4 to 20 °C. We hypothesized that intact soil microbial communities would exhibit shifts in pentose phosphate pathway and glycolysis activity in the same way as is regularly observed for individual microorganisms in pure culture. We also hypothesized that increased maintenance respiration at higher temperature would result in greater energy production and reduced carbon use efficiency (CUE). Two hours after temperature increase, respiration increased almost 10-fold. Although all metabolic processes were increased, the relative activity of metabolic processes, biosynthesis, and energy production changed. Pentose phosphate pathway was reduced (17-20{\%}), while activities of specific steps in glycolysis (51{\%}) and Krebs cycle (7-13{\%}) were increased. In contrast, only small but significant changes in biosynthesis (+2{\%}), ATP production (-3{\%}) and CUE (+2{\%}) were observed. In a second experiment, we compared the metabolic responses to temperature increases in soils from high and low elevation. The shift in activity from pentose phosphate pathway to glycolysis with higher temperature was confirmed in both soils, but the responses of Krebs cycle, biosynthesis, ATP production, and CUE were site dependent. Our results indicate that 1) in response to temperature, communities behave biochemically similarly to single species and, 2) our understanding of temperature effects on CUE, energy production and use for maintenance and growth processes is still incomplete.",
keywords = "C metabolism, Carbon, Glycolysis, Krebs cycle, Modeling, Pentose phosphate pathway, Soil microbial biomass, Stable isotopes, Temperature",
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TY - JOUR

T1 - Effect of temperature on metabolic activity of intact microbial communities

T2 - Evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency

AU - Dijkstra, Paul

AU - Thomas, Scott C.

AU - Heinrich, Paul L.

AU - Koch, George W

AU - Schwartz, Egbert

AU - Hungate, Bruce A

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N2 - We used metabolic tracers and modeling to analyze the response of soil metabolism to a sudden change in temperature from 4 to 20 °C. We hypothesized that intact soil microbial communities would exhibit shifts in pentose phosphate pathway and glycolysis activity in the same way as is regularly observed for individual microorganisms in pure culture. We also hypothesized that increased maintenance respiration at higher temperature would result in greater energy production and reduced carbon use efficiency (CUE). Two hours after temperature increase, respiration increased almost 10-fold. Although all metabolic processes were increased, the relative activity of metabolic processes, biosynthesis, and energy production changed. Pentose phosphate pathway was reduced (17-20%), while activities of specific steps in glycolysis (51%) and Krebs cycle (7-13%) were increased. In contrast, only small but significant changes in biosynthesis (+2%), ATP production (-3%) and CUE (+2%) were observed. In a second experiment, we compared the metabolic responses to temperature increases in soils from high and low elevation. The shift in activity from pentose phosphate pathway to glycolysis with higher temperature was confirmed in both soils, but the responses of Krebs cycle, biosynthesis, ATP production, and CUE were site dependent. Our results indicate that 1) in response to temperature, communities behave biochemically similarly to single species and, 2) our understanding of temperature effects on CUE, energy production and use for maintenance and growth processes is still incomplete.

AB - We used metabolic tracers and modeling to analyze the response of soil metabolism to a sudden change in temperature from 4 to 20 °C. We hypothesized that intact soil microbial communities would exhibit shifts in pentose phosphate pathway and glycolysis activity in the same way as is regularly observed for individual microorganisms in pure culture. We also hypothesized that increased maintenance respiration at higher temperature would result in greater energy production and reduced carbon use efficiency (CUE). Two hours after temperature increase, respiration increased almost 10-fold. Although all metabolic processes were increased, the relative activity of metabolic processes, biosynthesis, and energy production changed. Pentose phosphate pathway was reduced (17-20%), while activities of specific steps in glycolysis (51%) and Krebs cycle (7-13%) were increased. In contrast, only small but significant changes in biosynthesis (+2%), ATP production (-3%) and CUE (+2%) were observed. In a second experiment, we compared the metabolic responses to temperature increases in soils from high and low elevation. The shift in activity from pentose phosphate pathway to glycolysis with higher temperature was confirmed in both soils, but the responses of Krebs cycle, biosynthesis, ATP production, and CUE were site dependent. Our results indicate that 1) in response to temperature, communities behave biochemically similarly to single species and, 2) our understanding of temperature effects on CUE, energy production and use for maintenance and growth processes is still incomplete.

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KW - Carbon

KW - Glycolysis

KW - Krebs cycle

KW - Modeling

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KW - Soil microbial biomass

KW - Stable isotopes

KW - Temperature

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