TY - JOUR
T1 - A soil actinobacterium scavenges atmospheric H2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases
AU - Greening, Chris
AU - Berney, Michael
AU - Hards, Kiel
AU - Cook, Gregory M.
AU - Conrad, Ralf
PY - 2014/3/18
Y1 - 2014/3/18
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.
AB - 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.
KW - Atmospheric chemistry
KW - Biogeochemical cycles
KW - Enzyme kinetics
KW - Mycobacteria
UR - http://www.scopus.com/inward/record.url?scp=84896541745&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84896541745&partnerID=8YFLogxK
U2 - 10.1073/pnas.1320586111
DO - 10.1073/pnas.1320586111
M3 - Article
C2 - 24591586
AN - SCOPUS:84896541745
SN - 0027-8424
VL - 111
SP - 4257
EP - 4261
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 11
ER -