A nitrite-oxidizing bacterium constitutively consumes atmospheric hydrogen

Leung, Pok Man; Daebeler, Anne; Chiri, Eleonora; Cordero, Paul R. F.; Hanchapola, Iresha; Gillett, David L.; Schittenhelm, Ralf B.; Daims, Holger; Greening, Chris

doi:10.1101/2021.08.20.457082

Cited by 3 publications

(1 citation statement)

References 34 publications

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“…More recently, several high-affinity lineages of group 1 and 2 [NiFe]-hydrogenases have been identified that input atmospheric H 2 -derived electrons into the aerobic respiratory chain [4,5,21,29,30]. Whole-cell studies suggest these enzymes have a significantly higher apparent affinity for H 2 (K m 30 to 200 nM) and appear to be insensitive to inhibition by O 2 [4,5,10,12,13,31,32]. However, given these hydrogenases have yet to be isolated, it remains unknown how they have evolved to selectively oxidize H 2 , tolerate exposure to O 2 , and interact with the electron transport chain.…”

Section: Introductionmentioning

confidence: 99%

Energy extraction from air: structural basis of atmospheric hydrogen oxidation

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Kropp

Venugopal

et al. 2022

Preprint

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Diverse aerobic bacteria use atmospheric H2 as an energy source for growth and survival. This recently discovered yet globally significant process regulates the composition of the atmosphere, enhances soil biodiversity, and drives primary production in certain extreme environments. Atmospheric H2 oxidation has been attributed to still uncharacterised members of the [NiFe]-hydrogenase superfamily. However, it is unresolved how these enzymes overcome the extraordinary catalytic challenge of selectively oxidizing picomolar levels of H2 amid ambient levels of the catalytic poison O2, and how the derived electrons are transferred to the respiratory chain. Here we determined the 1.52 angstroms resolution CryoEM structure of the mycobacterial hydrogenase Huc and investigated its mechanism by integrating kinetics, electrochemistry, spectroscopy, mass spectrometry, and molecular dynamics simulations. Purified Huc is an oxygen-insensitive enzyme that couples the oxidation of atmospheric H2 at its large subunit to the hydrogenation of the respiratory electron carrier menaquinone at its small subunit. The enzyme uses a narrow hydrophobic gas channel to selectively bind atmospheric H2 at the expense of O2, while three [3Fe-4S] clusters and their unusual ligation by a D-histidine modulate the electrochemical properties of the enzyme such that atmospheric H2 oxidation is energetically feasible. Huc forms an 833 kDa complex composed of an octamer of catalytic subunits around a membrane-associated central stalk, which extracts and transports menaquinone a remarkable 94 angstroms from the membrane, enabling its reduction. These findings provide a mechanistic basis for the biogeochemically and ecologically critical process of atmospheric H2 oxidation. Through the first characterisation of a group 2 [NiFe]-hydrogenase, we also uncover a novel mode of energy coupling dependent on long-range quinone transport and pave way for the development of biocatalysts that oxidize H2 in ambient air.

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Section: Introductionmentioning

confidence: 99%

Energy extraction from air: structural basis of atmospheric hydrogen oxidation

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Kropp

Venugopal

et al. 2022

Preprint

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ComammoxNitrospirabacteria outnumber canonical nitrifiers irrespective of electron donor mode and availability in biofiltration systems

Vilardi

Cotto

Sevillano

et al. 2022

FEMS Microbiology Ecology

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Complete ammonia oxidizing bacteria coexist with canonical ammonia and nitrite oxidizing bacteria in a wide range of environments. Whether this is due to competitive or cooperative interactions, or a result of niche separation is not yet clear. Understanding the factors driving coexistence of nitrifiers is critical to manage nitrification processes occurring in engineered and natural ecosystems. In this study, microcosm-based experiments were used to investigate the impact of nitrogen source and loading on the population dynamics of nitrifiers in drinking water biofilter media. Shotgun sequencing of DNA followed by co-assembly and reconstruction of metagenome assembled genomes revealed clade A2 comammox bacteria were likely the primary nitrifiers within microcosms and increased in abundance over Nitrsomonas-like ammonia and Nitrospira-like nitrite oxidizing bacteria irrespective of nitrogen source type or loading. Changes in comammox bacterial abundance did not correlate with either ammonia or nitrite oxidizing bacterial abundance in urea amended systems where metabolic reconstruction indicated potential for cross feeding between ammonia and nitrite oxidizing bacteria. In contrast, comammox bacterial abundance demonstrated a negative correlation with nitrite oxidizers in ammonia amended systems. This suggests potentially weaker synergistic relationships between ammonia and nitrite oxidizers might enable comammox bacteria to displace nitrite oxidizers from complex nitrifying communities.

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Molecular hydrogen is an overlooked energy source for marine bacteria

Lappan

Shelley

Islam

et al. 2022

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Molecular hydrogen (H2) and carbon monoxide (CO) are supersaturated in seawater relative to the atmosphere and hence are readily accessible energy sources for marine microbial communities. Yet while marine CO oxidation is well-described, it is unknown whether seawater communities consume H2. Here we integrated genome-resolved metagenomics, biogeochemistry, thermodynamic modelling, and culture-based analysis to profile H2 and CO oxidation by marine bacteria. Based on analysis of 14 surface water samples, collected from three locations spanning tropical to subantarctic fronts, three uptake hydrogenase classes are prevalent in seawater and encoded by major marine families such as Rhodobacteraceae, Flavobacteriaceae, and Sphingomonadaceae. However, they are less abundant and widespread than carbon monoxide dehydrogenases. Consistently, microbial communities in surface waters slowly consumed H2 and rapidly consumed CO at environmentally relevant concentrations, with H2 oxidation most active in subantarctic waters. The cell-specific power from these processes exceed bacterial maintenance requirements and, for H2, can likely sustain growth of bacteria with low energy requirements. Concordantly, we show that the polar ultramicrobacterium Sphingopyxis alaskensis grows mixotrophically on H2 by expressing a group 2a [NiFe]-hydrogenase, providing the first demonstration of atmospheric H2 oxidation by a marine bacterium. Based on TARA Oceans metagenomes, genes for trace gas oxidation are globally distributed and are fourfold more abundant in deep compared to surface waters, highlighting that trace gases are important energy sources especially in energy-limited waters. Altogether, these findings show H2 is a significant energy source for marine communities and suggest that trace gases influence the ecology and biogeochemistry of oceans globally.

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A nitrite-oxidizing bacterium constitutively consumes atmospheric hydrogen

Cited by 3 publications

References 34 publications

Energy extraction from air: structural basis of atmospheric hydrogen oxidation

Energy extraction from air: structural basis of atmospheric hydrogen oxidation

ComammoxNitrospirabacteria outnumber canonical nitrifiers irrespective of electron donor mode and availability in biofiltration systems

Molecular hydrogen is an overlooked energy source for marine bacteria

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