Crystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimus

Abstract 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) represents one of several...

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Main Authors: Jerome Johnson, Bradley B. Tolar, Bilge Tosun, Yasuo Yoshikuni, Christopher A. Francis, Soichi Wakatsuki, Hasan DeMirci
Format: Article
Language:English
Published: Nature Portfolio 2024-10-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-06432-x
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author Jerome Johnson
Bradley B. Tolar
Bilge Tosun
Yasuo Yoshikuni
Christopher A. Francis
Soichi Wakatsuki
Hasan DeMirci
author_facet Jerome Johnson
Bradley B. Tolar
Bilge Tosun
Yasuo Yoshikuni
Christopher A. Francis
Soichi Wakatsuki
Hasan DeMirci
author_sort Jerome Johnson
collection DOAJ
description Abstract 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) represents one of several enzymes from this cycle that exhibit increased efficiency over crenarchaeal counterparts. This enzyme reduces energy requirements on the cell, reflecting thaumarchaeal success in adapting to low-nutrient environments. Here we show the structure of Nmar_0206 from Nitrosopumilus maritimus SCM1, which reveals a highly conserved interdomain linker loop between the CoA-binding and ATP-grasp domains. Phylogenetic analysis suggests the widespread prevalence of this loop and highlights both its underrepresentation within the PDB and structural importance within the (ATP-forming) acyl-CoA synthetase (ACD) superfamily. This linker is shown to have a possible influence on conserved interface interactions between domains, thereby influencing homodimer stability. These results provide a structural basis for the energy efficiency of this key enzyme in the modified 3HP/4HB cycle of Thaumarchaeota.
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spelling doaj-art-b0074faf961d4e1784f937a5b876db422025-08-20T02:11:54ZengNature PortfolioCommunications Biology2399-36422024-10-017111010.1038/s42003-024-06432-xCrystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimusJerome Johnson0Bradley B. Tolar1Bilge Tosun2Yasuo Yoshikuni3Christopher A. Francis4Soichi Wakatsuki5Hasan DeMirci6Department of Molecular Biology and Genetics, Koç UniversityDepartment of Earth System Science, Stanford UniversityDepartment of Molecular Biology and Genetics, Koç UniversityThe US DOE Joint Genome Institute, Lawrence Berkeley National LaboratoryDepartment of Earth System Science, Stanford UniversityDepartment of Structural Biology, Stanford UniversityDepartment of Molecular Biology and Genetics, Koç UniversityAbstract 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) represents one of several enzymes from this cycle that exhibit increased efficiency over crenarchaeal counterparts. This enzyme reduces energy requirements on the cell, reflecting thaumarchaeal success in adapting to low-nutrient environments. Here we show the structure of Nmar_0206 from Nitrosopumilus maritimus SCM1, which reveals a highly conserved interdomain linker loop between the CoA-binding and ATP-grasp domains. Phylogenetic analysis suggests the widespread prevalence of this loop and highlights both its underrepresentation within the PDB and structural importance within the (ATP-forming) acyl-CoA synthetase (ACD) superfamily. This linker is shown to have a possible influence on conserved interface interactions between domains, thereby influencing homodimer stability. These results provide a structural basis for the energy efficiency of this key enzyme in the modified 3HP/4HB cycle of Thaumarchaeota.https://doi.org/10.1038/s42003-024-06432-x
spellingShingle Jerome Johnson
Bradley B. Tolar
Bilge Tosun
Yasuo Yoshikuni
Christopher A. Francis
Soichi Wakatsuki
Hasan DeMirci
Crystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimus
Communications Biology
title Crystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimus
title_full Crystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimus
title_fullStr Crystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimus
title_full_unstemmed Crystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimus
title_short Crystal structure of the 4-hydroxybutyryl-CoA synthetase (ADP-forming) from nitrosopumilus maritimus
title_sort crystal structure of the 4 hydroxybutyryl coa synthetase adp forming from nitrosopumilus maritimus
url https://doi.org/10.1038/s42003-024-06432-x
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