Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2

Abstract

Microbial-mediated soil uptake accounts for ∼80% of the global tropospheric dihydrogen (H2) sinks. Studies conducted over the last three decades provide indirect evidences that H2 soil uptake is mediated by free soil hydrogenases or by unknown microorganisms that have a high affinity for H2. The exact nature of these hypothetical free soil enzymes or of H2-consuming microorganisms remains elusive because the activity has never been observed in pure culture. Here, we present the first aerobic microorganism able to consume tropospheric H2 at ambient levels. A dynamic microcosm chamber was developed to enrich a microbial consortium with a high affinity for H2, from which selected bacterial and fungal strains were isolated and tested for H2 uptake. Strain PCB7 had a H2 consumption activity that followed a Michaelis–Menten kinetics, with an apparent Km of 11 p.p.m.v. and a H2 threshold concentration <0.100 p.p.m.v., corresponding to the high-affinity uptake of tropospheric H2 observed in soil. 16S ribosomal RNA gene sequences showed that strain PCB7 is highly related to several Streptomyces species. H2 consumption occurred during the sporulation period of the bacterium. Addition of nickel increased the activity, suggesting that the enzymes involved in H2 consumption belong to the NiFe uptake class of hydrogenases. Because this is the first microorganism showing a high-affinity uptake of tropospheric H2, we anticipate that Streptomyces sp. PCB7 will become a model organism for the understanding of the environmental factors influencing H2 soil uptake.

A soil actinobacterium scavenges atmospheric H 2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases

“…We definitively confirm that group 5 [NiFe] hydrogenases can mediate high-affinity H 2 oxidation and provide strong support for the hypothesis that these enzymes are the principal sinks for atmospheric H 2 . The kinetic parameters of whole-cell H 2 oxidation by Hyd2, as observed in isolation in the Δhyd13 strain and deleted in the Δhyd2 strain, are very similar to the high-affinity processes observed in whole soil samples (9, 10) and cultured streptomycetes (12,15) (Fig. 4).…”

“…The first isolated highaffinity H 2 -oxidizer, Streptomyces sp. PCB7, can oxidize H 2 with Michaelis-Menten kinetics with an apparent K m ≤30 nM and a threshold concentration ≤0.1 nM (15)(16)(17). An earlier study demonstrated that Mycobacterium smegmatis can oxidize low concentrations of H 2 , but did not determine the affinity or threshold of this activity (18).…”

“…However, it has recently been shown that certain soil-dwelling actinomycetes are capable of scavenging H 2 at tropospheric concentrations (12,15). The first isolated highaffinity H 2 -oxidizer, Streptomyces sp.…”

Isotopic signatures of production and uptake of H<sub>2</sub> by soil

“…This remained the basic hypothesis of many further soil uptake studies (Conrad et al, 1983;Conrad and Seiler, 1985;Ehhalt and Rohrer, 2011;Guo and Conrad, 2008;Häring et al, 1994;Smith-Downey et al, 2006). However, Constant et al (2008a) were first to identify an aerobic microorganism (Streptomyces sp. PCB7) that can consume H 2 at tropospheric ambient mole fractions and suggested that active metabolic cells could be responsible for the soil uptake of H 2 rather than extracellular enzymes.…”

Hydrogen soil deposition at an urban site in Finland

“…Earlier field measurements were made by Conrad andSeiler (1980, 1985) in Germany and in Africa. Soil microbes and free soil enzymes are responsible for hydrogen uptake (Conrad, 1996;Constant et al, 2008Constant et al, , 2009, and soil hydrogenases that are responsible for hydrogen uptake have recently been extracted by Guo and Conrad (2008) and Constant et al (2008). Photochemical production and destruction of atmospheric hydrogen is hydroxyl radical controlled.…”