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. 2016 Mar;10(3):761-77.
doi: 10.1038/ismej.2015.153. Epub 2015 Sep 25.

Genomic and Metagenomic Surveys of Hydrogenase Distribution Indicate H2 Is a Widely Utilised Energy Source for Microbial Growth and Survival

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Free PMC article

Genomic and Metagenomic Surveys of Hydrogenase Distribution Indicate H2 Is a Widely Utilised Energy Source for Microbial Growth and Survival

Chris Greening et al. ISME J. .
Free PMC article

Abstract

Recent physiological and ecological studies have challenged the long-held belief that microbial metabolism of molecular hydrogen (H2) is a niche process. To gain a broader insight into the importance of microbial H2 metabolism, we comprehensively surveyed the genomic and metagenomic distribution of hydrogenases, the reversible enzymes that catalyse the oxidation and evolution of H2. The protein sequences of 3286 non-redundant putative hydrogenases were curated from publicly available databases. These metalloenzymes were classified into multiple groups based on (1) amino acid sequence phylogeny, (2) metal-binding motifs, (3) predicted genetic organisation and (4) reported biochemical characteristics. Four groups (22 subgroups) of [NiFe]-hydrogenase, three groups (6 subtypes) of [FeFe]-hydrogenases and a small group of [Fe]-hydrogenases were identified. We predict that this hydrogenase diversity supports H2-based respiration, fermentation and carbon fixation processes in both oxic and anoxic environments, in addition to various H2-sensing, electron-bifurcation and energy-conversion mechanisms. Hydrogenase-encoding genes were identified in 51 bacterial and archaeal phyla, suggesting strong pressure for both vertical and lateral acquisition. Furthermore, hydrogenase genes could be recovered from diverse terrestrial, aquatic and host-associated metagenomes in varying proportions, indicating a broad ecological distribution and utilisation. Oxygen content (pO2) appears to be a central factor driving the phylum- and ecosystem-level distribution of these genes. In addition to compounding evidence that H2 was the first electron donor for life, our analysis suggests that the great diversification of hydrogenases has enabled H2 metabolism to sustain the growth or survival of microorganisms in a wide range of ecosystems to the present day. This work also provides a comprehensive expanded system for classifying hydrogenases and identifies new prospects for investigating H2 metabolism.

Figures

Figure 1
Figure 1
Classification and phylogeny of hydrogenases. These neighbour-joining skeleton trees show the phylogenetic relationships of all 3286 hydrogenases identified in this work. The trees are colour coded by [NiFe]-hydrogenase subgroup and [FeFe]-hydrogenase group. The nodes separating the major clades are encircled and coloured according to their bootstrap values, that is, black circles for well-supported nodes (bootstrap values >0.75) and red circles for unsupported nodes (bootstrap values <0.75). Group A [FeFe]-hydrogenases cannot be reliably subdivided phylogenetically and can only be classified into subtypes based on their genetic organisation. The expanded trees, including taxon names and bootstrap values, are shown in Supplementary Figures S1 to S6.
Figure 2
Figure 2
Genetic organisation of hydrogenases. The genes surrounding the catalytic subunit of representatives of each subtype/subclass are shown to-scale. Genes/domains are colour coded as follows: green=catalytic site; blue=small subunit; yellow=electron acceptor or donor; red=redox subunit; light orange=maturation factor; dark orange=ion-translocation module; purple=regulatory module; grey=conserved hypothetical. Redox-active centres are shown in circles, where: orange=heme; red=[4Fe4S] cluster; yellow=[2Fe2S] cluster; green=[3Fe4S] cluster; purple=[4Fe3S] cluster. Genes are named according to nomenclature if previously defined. There are often variations in the genetic organisation within subgroups, for example, cytochrome c subunits replace cytochrome b subunits in most group 1a and 1b [NiFe]-hydrogenases in δ-Proteobacteria. However, the organisations depicted reflect the most common organisation, as inferred using the Microbial Genomic Context Viewer.
Figure 3
Figure 3
Distribution of hydrogenases in microorganisms. (a) Distribution by hydrogenase type. (b) Distribution by phyla. The cells are shaded by the number of hydrogenases detected in each phyla (light=few hydrogenases, dark=many hydrogenases, grey=no hydrogenases). Hydrogenases were subdivided into the following seven types based on their determined or predicted functions: [NiFe] aerobic uptake (groups 1d, 1h, 2a) [NiFe] anaerobic uptake (groups 1a, 1b, 1c, 1e, 1f, 1g, 3a), [NiFe] bidirectional (groups 3b, 3c, 3d), [NiFe] evolving (groups 4a, 4b, 4c, 4d, 4e, 4f), [FeFe] evolving (groups A, B), [NiFe] regulatory (groups 2b, 2c) and [FeFe] regulatory (group C).
Figure 4
Figure 4
Distribution of hydrogenases in ecosystems. The distribution of different hydrogenase types was analysed in 20 metagenomes. Hydrogenases were subdivided into seven types as described in the legend of Figure 3. Metagenomes were screened using the sequences of the catalytic subunits ([NiFe]-hydrogenases, [Fe]-hydrogenases) or catalytic domains ([FeFe]-hydrogenases) listed in Supplementary Table S1. (a) Percentage of sequence reads for each hydrogenase type identified within 1 million random metagenome reads. (b) Percentage of sequence reads for each hydrogenase type compared with total hydrogenase sequence reads. Supplementary Figure S5 shows the metagenome distribution by [NiFe]-hydrogenase subgroup and [FeFe]-hydrogenase group. Note that no [Fe]-hydrogenases were detected in these metagenomes.

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