A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases

Chris Greening, Michael Berney, Kiel Hards, Gregory M. Cook, Ralf Conrad

Research output: Contribution to journalArticle

49 Citations (Scopus)

Abstract

In the Earth's lower atmosphere, H2 is maintained at trace concentrations (0.53 ppmv/0.40 nM) and rapidly turned over (lifetime = 2.1 y-1). It is thought that soil microbes, likely actinomycetes, serve as the main global sink for tropospheric H2. However, no study has ever unambiguously proven that a hydrogenase can oxidize this trace gas. In this work, we demonstrate, by using genetic dissection and sensitive GC measurements, that the soil actinomycete Mycobacterium smegmatis mc2155 constitutively oxidizes subtropospheric concentrations of H2. We show that two membraneassociated, oxygen-dependent [NiFe] hydrogenases mediate this process. Hydrogenase-1 (Hyd1) (MSMEG-2262-2263) is well-adapted to rapidly oxidize H2 at a range of concentrations [Vmax(app) = 12 nmol.g.dw-1.min-1; Km(app) = 180 nM; threshold = 130 pM in the hyd23 (Hyd1 only) strain], whereas Hyd2 (MSMEG-2719-2720) catalyzes a slower-acting, higher-affinity process [Vmax(app) = 2.5 nmol.g.dw-1.min-1; Km(app) = 50 nM; threshold = 50 pM in the ?hyd13 (Hyd2 only) strain]. These observations strongly support previous studies that have linked group 5 [NiFe] hydrogenases (e. g., Hyd2) to the oxidation of tropospheric H2 in soil ecosystems. We further reveal that group 2a [NiFe] hydrogenases (e.g., Hyd1) can contribute to this process. Hydrogenase expression and activity increases in carbon-limited cells, suggesting that scavenging of trace H2 helps to sustain dormancy. Distinct physiological roles for Hyd1 and Hyd2 during the adaptation to this condition are proposed. Soil organisms harboring high-affinity hydrogenases may be especially competitive, given that they harness a highly dependable fuel source in otherwise unstable environments.

Original languageEnglish (US)
Pages (from-to)4257-4261
Number of pages5
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number11
DOIs
StatePublished - Mar 18 2014

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Hydrogenase
Actinobacteria
Soil
Oxygen
Membranes
Mycobacterium smegmatis
nickel-iron hydrogenase
Atmosphere
Ecosystem
Dissection
Carbon
Gases

Keywords

  • Atmospheric chemistry
  • Biogeochemical cycles
  • Enzyme kinetics
  • Mycobacteria

ASJC Scopus subject areas

  • General

Cite this

A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases. / Greening, Chris; Berney, Michael; Hards, Kiel; Cook, Gregory M.; Conrad, Ralf.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, No. 11, 18.03.2014, p. 4257-4261.

Research output: Contribution to journalArticle

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abstract = "In the Earth's lower atmosphere, H2 is maintained at trace concentrations (0.53 ppmv/0.40 nM) and rapidly turned over (lifetime = 2.1 y-1). It is thought that soil microbes, likely actinomycetes, serve as the main global sink for tropospheric H2. However, no study has ever unambiguously proven that a hydrogenase can oxidize this trace gas. In this work, we demonstrate, by using genetic dissection and sensitive GC measurements, that the soil actinomycete Mycobacterium smegmatis mc2155 constitutively oxidizes subtropospheric concentrations of H2. We show that two membraneassociated, oxygen-dependent [NiFe] hydrogenases mediate this process. Hydrogenase-1 (Hyd1) (MSMEG-2262-2263) is well-adapted to rapidly oxidize H2 at a range of concentrations [Vmax(app) = 12 nmol.g.dw-1.min-1; Km(app) = 180 nM; threshold = 130 pM in the hyd23 (Hyd1 only) strain], whereas Hyd2 (MSMEG-2719-2720) catalyzes a slower-acting, higher-affinity process [Vmax(app) = 2.5 nmol.g.dw-1.min-1; Km(app) = 50 nM; threshold = 50 pM in the ?hyd13 (Hyd2 only) strain]. These observations strongly support previous studies that have linked group 5 [NiFe] hydrogenases (e. g., Hyd2) to the oxidation of tropospheric H2 in soil ecosystems. We further reveal that group 2a [NiFe] hydrogenases (e.g., Hyd1) can contribute to this process. Hydrogenase expression and activity increases in carbon-limited cells, suggesting that scavenging of trace H2 helps to sustain dormancy. Distinct physiological roles for Hyd1 and Hyd2 during the adaptation to this condition are proposed. Soil organisms harboring high-affinity hydrogenases may be especially competitive, given that they harness a highly dependable fuel source in otherwise unstable environments.",
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AU - Berney, Michael

AU - Hards, Kiel

AU - Cook, Gregory M.

AU - Conrad, Ralf

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N2 - In the Earth's lower atmosphere, H2 is maintained at trace concentrations (0.53 ppmv/0.40 nM) and rapidly turned over (lifetime = 2.1 y-1). It is thought that soil microbes, likely actinomycetes, serve as the main global sink for tropospheric H2. However, no study has ever unambiguously proven that a hydrogenase can oxidize this trace gas. In this work, we demonstrate, by using genetic dissection and sensitive GC measurements, that the soil actinomycete Mycobacterium smegmatis mc2155 constitutively oxidizes subtropospheric concentrations of H2. We show that two membraneassociated, oxygen-dependent [NiFe] hydrogenases mediate this process. Hydrogenase-1 (Hyd1) (MSMEG-2262-2263) is well-adapted to rapidly oxidize H2 at a range of concentrations [Vmax(app) = 12 nmol.g.dw-1.min-1; Km(app) = 180 nM; threshold = 130 pM in the hyd23 (Hyd1 only) strain], whereas Hyd2 (MSMEG-2719-2720) catalyzes a slower-acting, higher-affinity process [Vmax(app) = 2.5 nmol.g.dw-1.min-1; Km(app) = 50 nM; threshold = 50 pM in the ?hyd13 (Hyd2 only) strain]. These observations strongly support previous studies that have linked group 5 [NiFe] hydrogenases (e. g., Hyd2) to the oxidation of tropospheric H2 in soil ecosystems. We further reveal that group 2a [NiFe] hydrogenases (e.g., Hyd1) can contribute to this process. Hydrogenase expression and activity increases in carbon-limited cells, suggesting that scavenging of trace H2 helps to sustain dormancy. Distinct physiological roles for Hyd1 and Hyd2 during the adaptation to this condition are proposed. Soil organisms harboring high-affinity hydrogenases may be especially competitive, given that they harness a highly dependable fuel source in otherwise unstable environments.

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