Trace gas oxidizers are widespread and active members of soil microbial communities

Bay, Sean K.; Dong, Xiyang; Bradley, James A.; Leung, Pok Man; Grinter, Rhys; Jirapanjawat, Thanavit; Arndt, Stefan K.; Cook, Perran; LaRowe, Douglas E.; Nauer, Philipp A.; Chiri, Eleonora; Greening, Chris

doi:10.1038/s41564-020-00811-w

Cited by 118 publications

(104 citation statements)

References 114 publications

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“…Our results show that M. capsulatus Bath is a chemoorganoautotroph that strongly prefers CH 4 as an energy source and requires both CH 4 and CO 2 as carbon sources. Further research is needed to understand why some methanotrophs encode RubisCO and assimilate CO 2 via a CBB cycle while others do not, but the metabolic plasticity afforded by the presence of hydrogenases, methane monooxygenases, and RubisCO may allow these microbes to inhabit and contribute to primary productivity in diverse habitats ( 2 , 32 , 33 ).…”

Section: Discussionmentioning

confidence: 99%

Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (RubisCO) Is Essential for Growth of the Methanotroph Methylococcus capsulatus Strain Bath

Henard

Xiong

et al. 2021

Appl Environ Microbiol

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The ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) enzyme found in plants, algae, and an array of autotrophic bacteria is also encoded by a subset of methanotrophs, but its role in these microbes has largely remained elusive. In this study, we identified that CO 2 was requisite for RubisCO-encoding Methylococcus capsulatus Bath growth in a bioreactor with continuous influent and effluent gas flow. RNA sequencing identified active transcription of several carboxylating enzymes, including key enzymes of the Calvin and serine cycles, that could mediate CO 2 assimilation during cultivation with both CH 4 and CO 2 as carbon sources. Marker-exchange mutagenesis of M. capsulatus Bath genes encoding key enzymes of potential CO 2 -assimilating metabolic pathways indicated that a complete serine cycle is not required while RubisCO is essential for growth of this bacterium. 13 CO 2 tracer analysis showed that CH 4 and CO 2 enter overlapping anaplerotic pathways and implicated RubisCO as the primary enzyme mediating CO 2 assimilation in M. capsulatus Bath. Notably, we quantified the relative abundance of 3-phosphoglycerate and ribulose-1,5-bisphosphate 13 C isotopes, which supported that RubisCO-produced 3-phosphoglycerate is primarily converted to ribulose-1-5-bisphosphate via the oxidative pentose phosphate pathway in M. capsulatus Bath. Collectively, our data establish that RubisCO and CO 2 play essential roles in M. capsulatus Bath metabolism. This study expands the known capacity of methanotrophs to fix CO 2 via RubisCO, which may play a more pivotal role in the Earth’s biogeochemical carbon cycling and greenhouse gas regulation than previously recognized. Further, M. capsulatus Bath and other CO 2 -assimilating methanotrophs represent excellent candidates for use in the bioconversion of biogas waste streams that consist of both CH 4 and CO 2 . Importance The importance of RubisCO and CO 2 in M. capsulatus Bath metabolism is unclear. In this study, we demonstrated that both CO 2 and RubisCO are essential for M. capsulatus Bath growth. 13 CO 2 tracing experiments supported that RubisCO mediates CO 2 fixation and a non-canonical Calvin cycle is active in this organism. Our study provides insights into the expanding knowledge of methanotroph metabolism and implicates dual CH 4 /CO 2 -utilizing bacteria as more important players in the biogeochemical carbon cycle than previously appreciated. In addition, M. capsulatus and other methanotrophs with CO 2 assimilation capacity represent candidate organisms for the development of biotechnologies to mitigate the two most abundant greenhouse gases CH 4 and CO 2 .

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Section: Discussionmentioning

confidence: 99%

Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (RubisCO) Is Essential for Growth of the Methanotroph Methylococcus capsulatus Strain Bath

Henard

Xiong

et al. 2021

Appl Environ Microbiol

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“…Patescibacteria 32,33 as well as two MAGs from the metabolically exible predatory phylum Bdellovibrionota (Supplementary 2) 34,35 . MAGs spanned known autotrophic phyla including those capable of atmospheric chemosynthesis (Actinobacteriota, Ca.…”

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confidence: 99%

Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts

Ray

Zaugg

Benaud

et al. 2021

Preprint

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Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, hydrogen oxidising bacteria support primary production through a novel carbon fixation process reliant on the chemoautotrophy-associated RuBisCO form IE. Here, biochemical assays show that atmospheric chemosynthesis occurs globally for primary production, contributing significantly to autotrophic carbon fixation throughout arid to hyperarid deserts in Antarctica, the high Arctic, and the Tibetan Plateau. Taxonomic and functional analyses were performed on 230 dereplicated medium-to-high quality metagenome-assembled genomes (MAGs) derived from 18 cold desert metagenomes and an additional 24,080 publicly available genomes. We infer that atmospheric chemosynthetic bacteria are widespread across environmental and clinical samples, increasing our knowledge of the bacterial phyla genetically capable of atmospheric chemosynthesis to seven, with key enzymes co-occurring within MAGs from four previously unidentified phyla; Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota. We informatically identify an additional group of high-affinity hydrogenases, group 1m [NiFe]-hydrogenase using phylogenetics, gene structure analysis and homology modelling and reveal substantial new genetic diversity within RuBisCO form IE (rbcL1E), and high-affinity groups 1h and 1l [NiFe]-hydrogenases. Finally, we conclude that atmospheric chemosynthesis is a global phenomenon, extending throughout and beyond cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental and clinical reservoirs.

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“…These bacteria each possess either high- or medium-affinity group 1h, 1f, or 2a [NiFe]-hydrogenases [16–18] that input electrons into aerobic respiratory chains. Bacterial atmospheric H 2 oxidation is also biogeochemically significant, contributing to the net loss of three quarters of the H 2 removed from the atmosphere each year [10]. In this study, we addressed the hypothesis that nitrite-oxidizing bacteria are also capable of oxidizing atmospheric H 2 .…”

Section: Introductionmentioning

confidence: 99%

“…While the concentration of atmospheric H2 (530 ppbv) is thought to be too low to support growth, this gas nevertheless serves as a dependable lifeline for long-term survival and can be a useful supplement during mixotrophic growth. This reflects its ubiquitous availability, high diffusibility, low activation energy, and high energy yield [9,10]. Culture-based studies have revealed bacteria from at least six phyla oxidize atmospheric H2, including various organotrophs, lithotrophs, and methanotrophs [11][12][13][14][15].…”

Section: Introductionmentioning

confidence: 99%

A nitrite-oxidizing bacterium constitutively consumes atmospheric hydrogen

Leung

Daebeler

Chiri

et al. 2021

Preprint

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Chemolithoautotrophic nitrite-oxidizing bacteria (NOB) of the genus Nitrospira contribute to nitrification in diverse natural environments and engineered systems. Nitrospira are thought to be well-adapted to substrate limitation owing to their high affinity for nitrite and capacity to use alternative energy sources. Here, we demonstrate that the canonical nitrite oxidizer Nitrospira moscoviensis oxidizes hydrogen (H2) below atmospheric levels using a high-affinity group 2a nickel-iron hydrogenase [Km(app) = 32 nM]. Atmospheric H2 oxidation occurred under both nitrite-replete and nitrite-deplete conditions, suggesting low-potential electrons derived from H2 oxidation promote nitrite-dependent growth and enable survival during nitrite limitation. Proteomic analyses confirmed the hydrogenase was abundant under both conditions and indicated extensive metabolic changes occur to reduce energy expenditure and growth under nitrite-deplete conditions. Respirometry analysis indicates the hydrogenase and nitrite oxidoreductase are bona fide components of the aerobic respiratory chain of N. moscoviensis, though they transfer electrons to distinct electron carriers in accord with the contrasting redox potentials of their substrates. Collectively, this study suggests atmospheric H2 oxidation enhances the growth and survival of NOB in amid variability of nitrite supply. These findings also extend the phenomenon of atmospheric H2 oxidation to a seventh phylum (Nitrospirota) and reveal unexpected new links between the global hydrogen and nitrogen cycles.

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Trace gas oxidizers are widespread and active members of soil microbial communities

Cited by 118 publications

References 114 publications

Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (RubisCO) Is Essential for Growth of the Methanotroph Methylococcus capsulatus Strain Bath

Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase (RubisCO) Is Essential for Growth of the Methanotroph Methylococcus capsulatus Strain Bath

Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts

A nitrite-oxidizing bacterium constitutively consumes atmospheric hydrogen

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