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Microbial oxidation of atmospheric trace gases

Abstract

The atmosphere has recently been recognized as a major source of energy sustaining life. Diverse aerobic bacteria oxidize the three most abundant reduced trace gases in the atmosphere, namely hydrogen (H2), carbon monoxide (CO) and methane (CH4). This Review describes the taxonomic distribution, physiological role and biochemical basis of microbial oxidation of these atmospheric trace gases, as well as the ecological, environmental, medical and astrobiological importance of this process. Most soil bacteria and some archaea can survive by using atmospheric H2 and CO as alternative energy sources, as illustrated through genetic studies on Mycobacterium cells and Streptomyces spores. Certain specialist bacteria can also grow on air alone, as confirmed by the landmark characterization of Methylocapsa gorgona, which grows by simultaneously consuming atmospheric CH4, H2 and CO. Bacteria use high-affinity lineages of metalloenzymes, namely hydrogenases, CO dehydrogenases and methane monooxygenases, to utilize atmospheric trace gases for aerobic respiration and carbon fixation. More broadly, trace gas oxidizers enhance the biodiversity and resilience of soil and marine ecosystems, drive primary productivity in extreme environments such as Antarctic desert soils and perform critical regulatory services by mitigating anthropogenic emissions of greenhouse gases and toxic pollutants.

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Fig. 1: Enzyme lineages responsible for trace gas oxidation.
Fig. 2: Contribution of trace gas oxidation to energy conservation and carbon assimilation processes during bacterial growth and survival.
Fig. 3: The structural and biochemical basis of atmospheric H2, CO and CH4 oxidation.
Fig. 4: Mediators and importance of atmospheric H2, CO and CH4 oxidation at the ecosystem level.

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Acknowledgements

The work described in this Review was supported by research grants from the Australian Research Council (DE170100310, DP180101762, DP200103074) and National Health & Medical Research Council (APP1178715). The authors were supported by National Health & Medical Research Council Emerging Leader Fellowships (APP1178715 to C.G.; APP1197376 to R.G.). The authors thank G. Berggren, D. Fox and K. Bayly for critically reading the manuscript.

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Glossary

Aerobic respiration

A process in which cells generate ATP through the oxidation of organic or inorganic compounds with oxygen (O2) as the terminal electron acceptor.

Primary production

The creation of new organic matter by fixing inorganic carbon (typically carbon dioxide (CO2)) using solar energy (photosynthesis) or chemical energy (chemosynthesis).

Trace gases

Gases that are in low concentrations in the atmosphere or other environments; in the atmosphere, this includes all gases other than nitrogen (N2), oxygen (O2) and argon.

Anthropogenic emissions

Gases produced and released into the atmosphere due to human activities, for example combusting fossil fuels and rearing ruminant livestock.

High-affinity enzymes

Enzymes capable of oxidizing low concentrations of substrates; enzymes with a high affinity for hydrogen (H2) or carbon monoxide (CO) (Km app < 150 nM), typically support long-term survival.

Carbon fixation

A biochemical process by which inorganic carbon (typically carbon dioxide (CO2)) is converted into organic compounds by chemosynthetic or photosynthetic organisms.

Biogeochemical cycling

A process by which chemical elements and compounds are cycled globally through a combination of biotic and abiotic processes, including those driven by anthropogenic activities.

Methane monooxygenases

Enzymes that use oxygen (O2) to convert methane (CH4) into methanol; subdivided into two unrelated families, the copper-dependent membrane-bound (particulate) methane monooxygenases (pMMOs) and iron-dependent soluble methane monooxygenases (sMMOs).

Hydrogenotrophs

Bacteria and archaea that grow chemolithoautotrophically by using hydrogen (H2) and carbon dioxide (CO2) as their sole energy, electron and carbon sources.

Carboxydotrophs

Bacteria that can grow chemolithoautotrophically by using carbon monoxide (CO) as the sole energy, electron and carbon source.

Methanotrophs

Bacteria and archaea that grow using methane (CH4) as their sole source of energy, electrons and, often, carbon.

Mixotrophic

Describes organisms that simultaneously use multiple nutritional strategies (for example, oxidation of both organic and inorganic energy sources) for growth or survival.

Organoheterotrophic

Organisms that grow by using organic compounds (for example, sugars) as their energy and carbon sources.

Metalloenzymes

Enzymes containing metal cofactors, which are directly bound to the protein.

Overpotential

The additional energy required over the energy that is thermodynamically predicted for a redox reaction to occur; this can depend on the activation energy of the reaction.

Electron donors

Molecules that donate electrons to another molecule during a redox reaction, for example NADH during organotrophic growth or hydrogen (H2) during lithotrophic growth.

Hydrogenase

A metalloenzyme that reversibly cleaves hydrogen (H2) into electrons and protons; they belong to three different classes, [NiFe]-hydrogenases, [FeFe]-hydrogenases and [Fe]-hydrogenases, which are variably distributed among bacteria, archaea and unicellular eukaryotes.

Carbon monoxide dehydrogenase

An enzyme that catalyses the reversible oxidation of carbon monoxide (CO) with water to carbon dioxide (CO2), two electrons and two protons; two unrelated enzymes families mediate this process, a molybdenum–copper enzyme found in aerobes and a nickel–iron enzyme found in anaerobes.

K m app

The apparent Michaelis constant of a reaction (that is, the concentration of a given substrate that catalyses the associated reaction at half the maximum rate), as observed in whole cells or environmental samples rather than purified enzymes.

Oxygen-insensitive hydrogenase

[NiFe]-hydrogenase that is not inhibited by oxygen (O2) and, hence, can function in oxic environments, including ambient conditions.

Oxygen-sensitive hydrogenase

[NiFe]-hydrogenase that is rapidly inhibited by oxygen (O2) and, hence, can only function in anoxic environments.

Dormant

A state in which an organism temporarily stops growth, replication and movement, resulting in reduced energy expenditure and increased long-term survival.

Maintenance

Energy-requiring processes required by a microorganism to maintain viability, for example macromolecular repair, cell wall maintenance, membrane potential conservation and extracellular sensing.

Copiotrophic

Relates to environments in which resources such as organic carbon are abundant, for example due to high primary production; also used to describe microorganisms adapted to such environments.

Catabolite repression

A system of genetic regulation in which bacteria repress other metabolic genes in the presence of their preferred carbon and energy source.

Response regulators

In two-component systems, DNA-binding proteins that receive signals from upstream sensory histidine kinases and, in turn, regulate transcription of a subset of genes.

Histidine kinases

In two-component systems, transmembrane enzymes that sense external signals (for example, oxygen (O2) for DosT) and activate downstream cytosolic response regulators (for example, DosR) through phosphorylation reactions.

Fermentative

Carrying out the partial oxidation of organic carbon, yielding ATP via substrate-level phosphorylation and end products (for example, hydrogen (H2), acetate, ethanol) that are excreted.

Cell-specific rates

The speeds at which a reaction occurs within single cells; in the case of trace gas oxidation, this can be estimated by dividing the rate at which a given sample consumes a trace gas by the number of microbial cells present that can consume it.

Lithoautotrophs

Bacteria and archaea that grow by using inorganic compounds (for example, hydrogen (H2) or carbon monoxide (CO)) to generate ATP and fix carbon dioxide (CO2) into biomass.

Carbon use efficiency

The proportion of organic carbon consumed by microorganisms used to generate biomass; this reflects the balance between anabolic and catabolic processes.

Anabolism

The biosynthesis of more complex compounds from simple chemical building blocks, typically in an ATP-dependent process.

Catabolism

The biological breakdown of compounds to yield energy to support cellular processes, typically resulting in the synthesis of ATP.

Reverse electron flow

A process in which an electron donor (for example, quinol) with a higher redox potential transfers electrons to an acceptor with lower potential (for example, NAD+) by consuming the proton-motive force to balance the energy deficit; this process is required for reductant generation and carbon fixation for many bacteria grown on high-potential energy sources, for example nitrite.

Respirometry

A general term for techniques that measure and interpret respiration rates in organisms, for example the measurement of microbial oxygen (O2) consumption using an O2 electrode.

Menaquinone

A lipid-soluble molecule produced by most bacteria and archaea that relays electrons from electron donors (for example, hydrogen (H2) via hydrogenases) to electron acceptors (for example, oxygen (O2) via cytochrome oxidases) in respiratory chains.

Membrane potential

The difference in electric potential between the interior and the exterior of a biological cell.

Electron acceptor

A molecule that receives electrons from another molecule during a redox reaction, for example oxygen (O2) during aerobic respiration or NO3 during anaerobic respiration.

Cytochrome bcc-aa 3 oxidase complex

A proton-translocating respiratory supercomplex, consisting of a cytochrome bcc-type quinone–cytochrome c oxidoreductase and a cytochrome aa3 oxidase, found in Actinobacteria.

Cytochrome bd oxidase

A terminal respiratory oxidase synthesized by many bacteria; compared with the cytochrome aa3 oxidase, it does not translocate protons resulting in lower energy yield but has a higher affinity for oxygen (O2) and resistance to respiratory chain inhibitors (including cyanide (CN), carbon monoxide (CO), nitric oxide (NO)).

Threshold

The lowest concentration of a substrate that can be used by an enzyme.

Proton-motive force

A proton gradient formed by electron transport chains that promotes proton flow and ATP synthesis by the F1Fo-ATP synthase; this is formed from a combination of concentration gradient (that is, pH difference) and an electrical gradient (that is, membrane potential).

Metabolic water

Water produced by cells during metabolic processes, largely from the reduction of oxygen (O2) during aerobic respiration.

Protomers

The smallest structural units of an oligomeric protein.

Oxygen-tolerant hydrogenases

[NiFe]-hydrogenases that are inhibited by oxygen (O2), but can readily reductively remove the bound O2 species and reactivate, and hence can function in micro-oxic environments.

Low-affinity enzymes

Enzymes capable of oxidizing high concentrations of a substrate; enzymes with a low affinity for hydrogen (H2), carbon monoxide (CO) or methane (CH4) (Km app > 500 nM), typically support lithoautotrophic growth.

Rare biosphere

A large number of microbial taxa that are present in very low numbers (<0.05% relative abundance) in most environments.

Metagenomic

Relating to DNA extracted and sequenced from a mixed community rather than a single population.

Metagenome-assembled genomes

Genomes of single taxa derived from the assembly and binning of one or more binned metagenomes.

Richness

The number of different taxa (species) present in a given ecosystem.

Turnover

In ecology, the number of different taxa (species) that are replaced in an ecosystem over different spatial or temporal scales.

Chemosynthetic

The fixation of carbon dioxide (CO2) into biomass using energy derived from chemical sources (for example, hydrogen (H2), carbon monoxide (CO)) by microorganisms.

RuBisCO

(Ribulose 1,5-bisphosphate carboxylase/oxygenase). An abundant enzyme that catalyses carbon dioxide (CO2) fixation through the Calvin–Benson cycle in chemosynthetic and photosynthetic organisms.

Biphasic kinetics

Biogeochemical processes in which two distinct kinetic activities simultaneously occur (for example, high-affinity and low-affinity trace gas oxidation in soils); typically mediated by different organisms and enzymes.

Oligotrophic

Relates to environments in which resources such as organic carbon are scarce, for example due to low primary production; also used to describe microorganisms adapted to such environments.

Photoautotrophs

Organisms that grow using light energy and electron donors (for example, water) to fix carbon dioxide (CO2) into biomass, including Cyanobacteria, algae and plants.

Primary succession

The colonization of a newly formed environment, for example formed from lava flow or glacial retreat, for the first time.

Exoplanets

Planets found outside the solar system.

Planetary protection

A guiding principle in the design of an interplanetary mission, aiming to prevent biological contamination of both the target celestial body and the Earth.

Abiogenesis

The emergence of biological life from chemical building blocks, estimated to have occurred ~3.5 billion years ago.

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Greening, C., Grinter, R. Microbial oxidation of atmospheric trace gases. Nat Rev Microbiol 20, 513–528 (2022). https://doi.org/10.1038/s41579-022-00724-x

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