Editorial: Microbial Hydrogen Metabolism

Greening, Chris; Boyd, Eric S.

doi:10.3389/fmicb.2020.00056

Cited by 8 publications

(6 citation statements)

References 57 publications

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“…Overall, the results suggest that H 2 metabolism is an ancestral and conserved trait of the class Chlorobia. This is also consistent with the widespread distribution of [NiFe]-hydrogenases across bacterial phyla (51,52) and the conservation of group 1d lineages in sister classes within the phylum Bacteroidota.…”

Section: Figsupporting

confidence: 85%

Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations

et al. 2021

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Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on the functional ecology and local adaptations of Chlorobia members came from isolates and merely 26 sequenced genomes that may not adequately represent natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-amplified genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs or “species”). Of the 71 mOTUs, 57 were classified within the genus Chlorobium, and these mOTUs represented up to ∼60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed, whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many lacked genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insight into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems. IMPORTANCE The reconstruction of genomes from metagenomes has helped explore the ecology and evolution of environmental microbiota. We applied this approach to 274 metagenomes collected from diverse freshwater habitats that spanned oxic and anoxic zones, sampling seasons, and latitudes. We demonstrate widespread and abundant distributions of planktonic Chlorobia-associated bacteria in hypolimnetic waters of stratified freshwater ecosystems and show they vary in their capacities to use different electron donors. Having photoautotrophic potential, these Chlorobia members could serve as carbon sources that support metalimnetic and hypolimnetic food webs.

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Section: Figsupporting

confidence: 85%

Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations

et al. 2021

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“…Overall, the results suggest that H 2 metabolism is an ancestral and conserved trait of the class Chlorobia. This is also consistent with the widespread distribution of [NiFe]-hydrogenases across bacterial phyla(51,52) and the conservation of3 group 1d lineages in sister classes of the phylum Bacteroidota.…”

supporting

confidence: 85%

FreshwaterChlorobiaexhibit metabolic specialization among cosmopolitan and endemic populations

Garcia

Mehrshad

Buck

et al. 2020

Preprint

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Photosynthetic bacteria from the class Chlorobia (formerly phylum Chlorobi) sustain carbon fixation in anoxic water columns. They harvest light at extremely low intensities and use various inorganic electron donors to fix carbon dioxide into biomass. Until now, most information on their functional ecology and local adaptations came from isolates and merely 26 sequenced genomes that are poor representatives of natural populations. To address these limitations, we analyzed global metagenomes to profile planktonic Chlorobia cells from the oxyclines of 42 freshwater bodies, spanning subarctic to tropical regions and encompassing all four seasons. We assembled and compiled over 500 genomes, including metagenome-assembled genomes (MAGs), single-cell genomes (SAGs), and reference genomes from cultures, clustering them into 71 metagenomic operational taxonomic units (mOTUs) or "species". Of the 71 mOTUs, 57 were classified as genus Chlorobium and these mOTUs varied in relative abundance up to ~60% of the microbial communities in the sampled anoxic waters. Several Chlorobium-associated mOTUs were globally distributed whereas others were endemic to individual lakes. Although most clades encoded the ability to oxidize hydrogen, many were lacking genes for the oxidation of specific sulfur and iron substrates. Surprisingly, one globally distributed Scandinavian Chlorobium clade encoded the ability to oxidize hydrogen, sulfur, and iron, suggesting that metabolic versatility facilitated such widespread colonization. Overall, these findings provide new insights into the biogeography of the Chlorobia and the metabolic traits that facilitate niche specialization within lake ecosystems.

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“…Microorganisms produce H 2 by using the [NiFe]-hydrogenase (Groups 3b and 4d) or [FeFe]-hydrogenase ( Greening et al 2016 ; Søndergaard et al 2016 ). These H 2 producers contribute to the major biogenic pool of H 2 on Earth (e.g., anoxic sediments and gastrointestinal tracts) ( Greening and Boyd 2020 ). In Thermoprofundales, the production of H 2 is catalyzed by the MBH-type [NiFe] hydrogenase, and reduced ferredoxin is the natural electron donor of this enzyme ( Yu et al 2018 ).…”

Section: Resultsmentioning

confidence: 99%

An Ancient Respiratory System in the Widespread Sedimentary Archaea Thermoprofundales

Zhang

Huang

Liu

et al. 2022

Molecular Biology and Evolution

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Thermoprofundales, formerly Marine Benthic Group D (MBG-D), is a ubiquitous archaeal lineage found in sedimentary environments worldwide. However, its taxonomic classification, metabolic pathways, and evolutionary history are largely unexplored because of its uncultivability and limited number of sequenced genomes. In this study, phylogenomic analysis and average amino acid identity values of a collection of 146 Thermoprofundales genomes revealed five Thermoprofundales subgroups (A-E) with distinct habitat preferences. Most of the microorganisms from Subgroups B and D were thermophiles inhabiting hydrothermal vents and hot spring sediments, whereas those from Subgroup E were adapted to surface environments where sunlight is available. H2 production may be featured in Thermoprofundales as evidenced by a gene cluster encoding the ancient membrane-bound hydrogenase (MBH) complex. Interestingly, a unique structure separating the MBH gene cluster into two modular units was observed exclusively in the genomes of Subgroup E, which included a peripheral arm encoding the [NiFe] hydrogenase domain and a membrane arm encoding the Na+/H+ antiporter domain. These two modular structures were confirmed to function independently by detecting the H2-evolving activity in vitro and salt tolerance to 0.2 M NaCl in vivo, respectively. The peripheral arm of Subgroup E resembles the proposed common ancestral respiratory complex of modern respiratory systems, which plays a key role in the early evolution of life. In addition, molecular dating analysis revealed that Thermoprofundales is an early emerging archaeal lineage among the extant MBH-containing microorganisms, indicating new insights into the evolution of this ubiquitous archaea lineage.

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Editorial: Microbial Hydrogen Metabolism

Cited by 8 publications

References 57 publications

Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations

Freshwater Chlorobia Exhibit Metabolic Specialization among Cosmopolitan and Endemic Populations

FreshwaterChlorobiaexhibit metabolic specialization among cosmopolitan and endemic populations

An Ancient Respiratory System in the Widespread Sedimentary Archaea Thermoprofundales

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