Soils contain two different activities for oxidation of hydrogen

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100

fWe have known for 40 years that soils can consume the trace amounts of molecular hydrogen (H 2 ) found in the Earth's atmosphere. This process is predicted to be the most significant term in the global hydrogen cycle. However, the organisms and enzymes responsible for this process were only recently identified. Pure culture experiments demonstrated that several species of Actinobacteria, including streptomycetes and mycobacteria, can couple the oxidation of atmospheric H 2 to the reduction of ambient O 2 . A combination of genetic, biochemical, and phenotypic studies suggest that these organisms primarily use this fuel source to sustain electron input into the respiratory chain during energy starvation. This process is mediated by a specialized enzyme, the group 5 [NiFe]-hydrogenase, which is unusual for its high affinity, oxygen insensitivity, and thermostability. Atmospheric hydrogen scavenging is a particularly dependable mode of energy generation, given both the ubiquity of the substrate and the stress tolerance of its catalyst. This minireview summarizes the recent progress in understanding how and why certain organisms scavenge atmospheric H 2 . In addition, it provides insight into the wider significance of hydrogen scavenging in global H 2 cycling and soil microbial ecology.

Section: Discussionmentioning

confidence: 99%

Atmospheric Hydrogen Scavenging: from Enzymes to Ecosystems

Greening

Constant

Hards

et al. 2015

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100

“…After centrifugation of the fully grown cultures, the cell-free supernatants were acidified with H 2 SO 4 (50 mM final concentration) and analyzed by high-performance liquid chromatography (HPLC) with an ion-exclusion column (Resin H ϩ IEX column, 8 m; Grom, Rottenburg, Germany) and a refractive index detector (27). The hydrogen concentration in the culture headspaces was analyzed by gas chromatography with a thermal conductivity detector (44).…”

Section: Methodsmentioning

confidence: 99%

Oxygen Affects Gut Bacterial Colonization and Metabolic Activities in a Gnotobiotic Cockroach Model

Tegtmeier

Thompson

Schauer

et al. 2016

The gut microbiota of termites and cockroaches represents complex metabolic networks of many diverse microbial populations. The distinct microenvironmental conditions within the gut and possible interactions among the microorganisms make it essential to investigate how far the metabolic properties of pure cultures reflect their activities in their natural environment. We established the cockroach Shelfordella lateralis as a gnotobiotic model and inoculated germfree nymphs with two bacterial strains isolated from the guts of conventional cockroaches. Fluorescence microscopy revealed that both strains specifically colonized the germfree hindgut. In diassociated cockroaches, the facultatively anaerobic strain EbSL (a new species of Enterobacteriaceae) always outnumbered the obligately anaerobic strain FuSL (a close relative of Fusobacterium varium), irrespective of the sequence of inoculation, which showed that precolonization by facultatively anaerobic bacteria does not necessarily favor colonization by obligate anaerobes. Comparison of the fermentation products of the cultures formed in vitro with those accumulated in situ indicated that the gut environment strongly affected the metabolic activities of both strains. The pure cultures formed the typical products of mixed-acid or butyrate fermentation, whereas the guts of gnotobiotic cockroaches accumulated mostly lactate and acetate. Similar shifts toward more-oxidized products were observed when the pure cultures were exposed to oxygen, which corroborated the strong effects of oxygen on the metabolic fluxes previously observed in termite guts. Oxygen microsensor profiles of the guts of germfree, gnotobiotic, and conventional cockroaches indicated that both gut tissue and microbiota contribute to oxygen consumption and suggest that the oxygen status influences the colonization success. M any insects, particularly those feeding on a fiber-rich diet, possess a dense and complex microbiota. The most prominent examples are termites, whose ability to thrive on an entirely lignocellulosic diet depends on the digestive and nutritional contributions of microbial symbionts housed in their intestinal tracts (1, 2). During recent years, the microbial community structure of many termites has been studied in detail, and the evolutionary patterns in the gut microbiota of termites and their closest phylogenetic relatives, the cockroaches, are slowly emerging (3). In particular, the application of high-throughput sequencing techniques provides sufficient resolution and sampling depth to distinguish the phylogenetic and environmental drivers of the community structure (4,5,6).The functional roles of individual community members and their interactions, however, are more difficult to elucidate, mostly due to their formidable resistance to cultivation. Metagenomic and metatranscriptomic approaches have provided the first insights into the functional potentials of the gut community (7,8,9), but owing to the lack of reference genomes for many deepbranching lineages of the gut microbiot...

“…Standard H 2 gas (1,000 ppmv Ϯ 2%; Messer Schweiz AG, Switzerland) was then added to the headspace of the bottles to obtain an initial mixing ratio of 1.5 to 1.8 ppmv H 2 . The decrease in the H 2 mixing ratio was monitored as a function of time by analyzing aliquots (0.5 ml) of the headspace air in a gas chromatograph with a reduction gas detector as described previously (49). Vials were continuously agitated at 100 rpm on an orbital shaker kept at 25°C to enhance the transfer of H 2 from the gas to the liquid phase.…”

Section: Methodsmentioning

confidence: 99%

Genome Data Mining and Soil Survey for the Novel Group 5 [NiFe]-Hydrogenase To Explore the Diversity and Ecological Importance of Presumptive High-Affinity H ₂ -Oxidizing Bacteria

Constant

Chowdhury

Hesse

et al. 2011

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119

Streptomyces soil isolates exhibiting the unique ability to oxidize atmospheric H 2 possess genes specifying a putative high-affinity [NiFe]-hydrogenase. This study was undertaken to explore the taxonomic diversity and the ecological importance of this novel functional group. We propose to designate the genes encoding the small and large subunits of the putative high-affinity hydrogenase hhyS and hhyL, respectively. Genome data mining revealed that the hhyL gene is unevenly distributed in the phyla Actinobacteria, Proteobacteria, Chloroflexi, and Acidobacteria. The hhyL gene sequences comprised a phylogenetically distinct group, namely, the group 5 [NiFe]-hydrogenase genes. The presumptive high-affinity H 2 -oxidizing bacteria constituting group 5 were shown to possess a hydrogenase gene cluster, including the genes encoding auxiliary and structural components of the enzyme and four additional open reading frames (ORFs) of unknown function. A soil survey confirmed that both high-affinity H 2 oxidation activity and the hhyL gene are ubiquitous. A quantitative PCR assay revealed that soil contained 10 6 to 10 8 hhyL gene copies g (dry weight) ؊1 . Assuming one hhyL gene copy per genome, the abundance of presumptive high-affinity H 2 -oxidizing bacteria was higher than the maximal population size for which maintenance energy requirements would be fully supplied through the H 2 oxidation activity measured in soil. Our data indicate that the abundance of the hhyL gene should not be taken as a reliable proxy for the uptake of atmospheric H 2 by soil, because high-affinity H 2 oxidation is a facultatively mixotrophic metabolism, and microorganisms harboring a nonfunctional group 5 [NiFe]-hydrogenase may occur.