Structural insights into bifunctional thaumarchaeal crotonyl-CoA hydratase and 3-hydroxypropionyl-CoA dehydratase from Nitrosopumilus maritimus

Destan, Ebru; Yüksel, Büşra; Tolar, Bradley B.; Ayan, Esra; Deutsch, Sam; Yoshikuni, Yasuo; Wakatsuki, Soichi; Francis, Christopher A.; DeMi̇rci̇, Hasan

doi:10.1038/s41598-021-02180-8

Cited by 6 publications

(3 citation statements)

References 37 publications

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“…The HP/HB cycle was first discovered in the thermoacidophilic, iron-oxidizing archaeon Metallosphaera sedula ( 65 ) and has been more recently described in detail for the ammonium-oxidizing archaeaon Nitrosopumilus maritimus ( 66 , 67 ). So far, this cycle has only been reported for the Archaea .…”

Section: Resultsmentioning

confidence: 99%

Carbon fixation pathways across the bacterial and archaeal tree of life

2022

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Carbon fixation is a critical process for our planet, however, its distribution across the bacterial and archaeal domains of life has not been comprehensively studied. Here, we performed an analysis of 52,515 metagenome-assembled genomes (MAGs) and discover carbon fixation pathways in 1007 bacteria and archaea. We reveal the genomic potential for carbon fixation through the reverse tricarboxylic acid cycle in previously unrecognised archaeal and bacterial phyla (ie. Thermoplasmatota and Elusimicrobiota) and show that the 3-hydroxypropionate bi-cycle is not, as previously thought, restricted to the phylum Chloroflexota. The data also substantially expands the phylogenetic breadth for autotrophy through the dicarboxylate/4-hydroxybutyrate cycle and the Calvin-Benson-Bassham cycle. Finally, the genomic potential for carbon fixation through the 4-hydroxybutyrate/3-hydroxypropionate cycle, previously exclusively found in Archaea, was also detected in the Bacteria. Carbon fixation appears thus to be much more widespread than previously known and this study lays the foundation to better understand the role of archaea and bacteria in global primary production and how they contribute to microbial carbon sinks.

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Section: Resultsmentioning

confidence: 99%

Carbon fixation pathways across the bacterial and archaeal tree of life

2022

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“…In the microbial ecosystem of Fe-Mn crusts and layers [ 26 ] a high proportion of members of Nitrososphaeria in communities suggests their significant role as primary producers. The oxidation of ammonia (Amo) and urea (Ure), as well as CO 2 (3HP/4HB) fixation, were predicted as possible for the Crenarchaeota-m3 MAG from Lake Baikal [ 111 ], which indicated their chemolithoautotrophic potential. As shown in Gabello-Yeves et al [ 112 ], genes associated with the N-cycle are more common in microorganisms inhabiting the deep area of the Baikal pelagic zone.…”

Section: Discussionmentioning

confidence: 99%

Microbial Communities in Ferromanganese Sediments from the Northern Basin of Lake Baikal (Russia)

et al. 2023

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We analyzed the amplicons of the 16S rRNA genes and assembled metagenome-assembled genomes (MAGs) of the enrichment culture from the Fe-Mn layer to have an insight into the diversity and metabolic potential of microbial communities from sediments of two sites in the northern basin of Lake Baikal. Organotrophic Chloroflexota, Actionobacteriota, and Acidobacteriota, as well as aerobic and anaerobic participants of the methane cycle (Methylococcales and Methylomirabilota, respectively), dominated the communities of the surface layers. With depth, one of the cores showed a decrease in the proportion of the Chloroflexota and Acidobacteriota members and a substantial increase in the sequences of the phylum Firmicutes. The proportion of the Desulfobacteriota and Thermodesulfovibronia (Nitrospirota) increased in another core. The composition of archaeal communities was similar between the investigated sites and differed in depth. Members of ammonia-oxidizing archaea (Nitrososphaeria) predominated in the surface sediments, with an increase in anaerobic methanotrophs (Methanoperedenaceae) and organoheterotrophs (Bathyarchaeia) in deep sediments. Among the 37 MAGs, Gammaproteobacteria, Desulfobacteriota, and Methylomirabilota were the most common in the microbial community. Metagenome sequencing revealed the assembled genomes genes for N, S, and CH4 metabolism for carbon fixation, and genes encoding Fe and Mn pathways, indicating the likely coexistence of the biogeochemical cycle of various elements and creating certain conditions for the development of taxonomically and functionally diverse microbial communities.

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“…The enzymes involved in the 3HP/4HB cycle have been selected for energy-efficient attributes, such as the bifunctionality of crotonyl-CoA hydratase/3-hydroxypropionyl-CoA dehydratase 24 and the oxygen-tolerance of 4-hydroxybutyryl-CoA dehydratase 25 . The growing demand for carbon fixation strategies to remediate our rapidly changing atmosphere begs for further tools, such as those which can be produced from the analysis of highly efficient enzymes.…”

Section: Summary/conclusionmentioning

confidence: 99%

Crystal Structure of 4-Hydroxybutyryl-CoA Synthetase (ADP-forming): A Key Enzyme in the Thaumarchaeal Hydroxypropionate/Hydroxybutyrate cycle

DeMi̇rci̇

Johnson²,

Tolar³

et al. 2023

Preprint

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The 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) cycle from ammonia-oxidizing Thaumarchaeota is currently considered the most energy-efficient aerobic carbon fixation pathway. The Nitrosopumilus maritimus 4-hydroxybutyryl-CoA synthetase (ADP-forming) (Nmar_0206) from this cycle represents one of a number of proteins that exhibit increased efficiency over its crenarchaeal counterparts. Nmar_0206 catalyzes the conversion of 4-hydroxybutyrate (4HB) and Coenzyme-A (CoA) to 4-hydroxybutyryl-CoA through the dephosphorylation of ATP to ADP, as opposed to AMP as seen in Crenarchaeota. This enzyme reduces energy requirements on the cell, thus reflecting thaumarchaeal success in adapting to low-nutrient environments.

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Structural insights into bifunctional thaumarchaeal crotonyl-CoA hydratase and 3-hydroxypropionyl-CoA dehydratase from Nitrosopumilus maritimus

Cited by 6 publications

References 37 publications

Carbon fixation pathways across the bacterial and archaeal tree of life

Carbon fixation pathways across the bacterial and archaeal tree of life

Microbial Communities in Ferromanganese Sediments from the Northern Basin of Lake Baikal (Russia)

Crystal Structure of 4-Hydroxybutyryl-CoA Synthetase (ADP-forming): A Key Enzyme in the Thaumarchaeal Hydroxypropionate/Hydroxybutyrate cycle

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