Crystal structure of mevalonate 3,5-bisphosphate decarboxylase reveals insight into the evolution of decarboxylases in the mevalonate metabolic pathways

Aoki, Mizuki; Vinokur, J.M.; Motoyama, Kento; Ishikawa, Rino; Collazo, Michael; Cascio, Duilio; Sawaya, M.R.; Ito, Tomokazu; Bowie, James U.; Hemmi, Hisashi

doi:10.1016/j.jbc.2022.102111

Cited by 6 publications

(10 citation statements)

References 42 publications

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“…Moreover, the majority of the archaeal lineages use AcnX1, AcnX2 and AMPD to synthesize isoprenoids through the archaea-type MVA pathway (Figure 1a), which was recently discovered and proposed as the evolutionary prototype for the three other types [19,25]. Here, our comprehensive investigation further confirmed that the archaea-type is the most universal MVA pathway in archaea, including the majority of DPANN and Asgard archaea (Figure 1b).…”

Section: The Archaeal Origin Of the Mva Pathwaysupporting

confidence: 78%

“…The haloarchaea-type MVA pathway is thought to have evolved relatively late from the archaea-type pathway [19,25] due to its limited distribution in the aerobic halophiles from the class Haloarchaeia and some Chloroflexota [12,13]. Here, our work remarkably expanded the distribution of the haloarchaea-type MVA pathway in the domain Archaea by finding its key enzyme PMD in phyla Thermoplasmatota, Thermoproteota, and Asgardarchaeota (Figure 1b), along with rather conserved phylogeny on the trees (Figure S3b).…”

Section: The Evolution Of the Haloarchaea-type And Thermoplasma-type ...mentioning

confidence: 60%

“…Nonetheless, some researchers suggest that the phylogenetic position of CPR, upon which the inference relies, may not be situated at the root of the bacterial tree of life [23,24]. In addition, the recently discovered archaea-type MVA pathway is supposed to be suitable for anaerobic life owing to the lesser consumption of energy and is thus inferred as the prototype for all other types, which subsequently evolved into the haloarchaea-type pathway, followed by the eukaryote-type and the Thermoplasma-type, respectively [19,25]. Therefore, the debatable basal phylogenic position of CPR in the bacterial tree of life and the emergence of the putative prototype for the MVA pathway make the origin and evolutionary history of the MVA pathway remain controversial.…”

Section: Introductionmentioning

confidence: 99%

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Expanded Archaeal Genomes Shed New Light on the Evolution of Isoprenoid Biosynthesis

Zhu,

Hou,

Xiong

et al. 2024

Microorganisms

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Isoprenoids and their derivatives, essential for all cellular life on Earth, are particularly crucial in archaeal membrane lipids, suggesting that their biosynthesis pathways have ancient origins and play pivotal roles in the evolution of early life. Despite all eukaryotes, archaea, and a few bacterial lineages being known to exclusively use the mevalonate (MVA) pathway to synthesize isoprenoids, the origin and evolutionary trajectory of the MVA pathway remain controversial. Here, we conducted a thorough comparison and phylogenetic analysis of key enzymes across the four types of MVA pathway, with the particular inclusion of metagenome assembled genomes (MAGs) from uncultivated archaea. Our findings support an archaeal origin of the MVA pathway, likely postdating the divergence of Bacteria and Archaea from the Last Universal Common Ancestor (LUCA), thus implying the LUCA’s enzymatic inability for isoprenoid biosynthesis. Notably, the Asgard archaea are implicated in playing central roles in the evolution of the MVA pathway, serving not only as putative ancestors of the eukaryote- and Thermoplasma-type routes, but also as crucial mediators in the gene transfer to eukaryotes, possibly during eukaryogenesis. Overall, this study advances our understanding of the origin and evolutionary history of the MVA pathway, providing unique insights into the lipid divide and the evolution of early life.

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Section: The Archaeal Origin Of the Mva Pathwaysupporting

confidence: 78%

Section: The Evolution Of the Haloarchaea-type And Thermoplasma-type ...mentioning

confidence: 60%

Section: Introductionmentioning

confidence: 99%

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Expanded Archaeal Genomes Shed New Light on the Evolution of Isoprenoid Biosynthesis

Zhu,

Hou,

Xiong

et al. 2024

Microorganisms

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“…( R )-mevalonate 3-phosphate was synthesized from ( R )-mevalonate by phosphorylation catalyzed by mevalonate 3-kinase Ta1305 [ 94 , 122 ]. ( R )-mevalonate 3,5-bisphosphate has been prepared from ( R )-mevalonate by a first phosphorylation catalyzed by mevalonate 3-kinase Ta1305, followed by a second phosphorylation catalyzed by mevalonate 3-phosphate 5-kinase Ta0762 [ 123 , 124 ], or by the E140 mutants which convert the mevalonate 3-kinase into a mevalonate 3-phosphate 5-kinase by replacing a glutamate residue interacting with the substrate by smaller amino acids [ 124 ]. Shikimate-3-phosphate lithium salt was prepared with >97% purity and 53% yield by highly efficient and selective phosphorylation of shikimate in one reaction step catalyzed by recombinant shikimate kinase AroL from E. coli [ 125 , 126 ].…”

Section: Synthesis Of Biologically Active Phosphometabolitesmentioning

confidence: 99%

Advances in the Synthesis and Analysis of Biologically Active Phosphometabolites

Wohlgemuth

2023

IJMS

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Phosphorus-containing metabolites cover a large molecular diversity and represent an important domain of small molecules which are highly relevant for life and represent essential interfaces between biology and chemistry, between the biological and abiotic world. The large but not unlimited amount of phosphate minerals on our planet is a key resource for living organisms on our planet, while the accumulation of phosphorus-containing waste is associated with negative effects on ecosystems. Therefore, resource-efficient and circular processes receive increasing attention from different perspectives, from local and regional levels to national and global levels. The molecular and sustainability aspects of a global phosphorus cycle have become of much interest for addressing the phosphorus biochemical flow as a high-risk planetary boundary. Knowledge of balancing the natural phosphorus cycle and the further elucidation of metabolic pathways involving phosphorus is crucial. This requires not only the development of effective new methods for practical discovery, identification, and high-information content analysis, but also for practical synthesis of phosphorus-containing metabolites, for example as standards, as substrates or products of enzymatic reactions, or for discovering novel biological functions. The purpose of this article is to review the advances which have been achieved in the synthesis and analysis of phosphorus-containing metabolites which are biologically active.

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“…tAHMP is then decarboxylated and phosphorylated to yield isopentenyl diphosphate, a common precursor for the biosynthesis of isoprenoids, such as archaeal membrane lipids. This pathway is utilized by archaea, excluding some exceptions such as halophilic archaea of the class Halobacteria ( Dellas et al, 2013 ; VanNice et al, 2014 ) and thermoacidophilic archaea of the orders Sulfolobales ( Nishimura et al, 2013 ) and Thermoplasmatales ( Azami et al, 2014 ; Vinokur et al, 2014 , 2015 , 2016 ; Rossoni et al, 2015 ; Aoki et al, 2022 ); therefore, it is considered the evolutionary prototype of the eukaryotic, haloarchaea, and Thermoplasma -type MVA pathways ( Hayakawa et al, 2018 ; Aoki et al, 2022 ). The archaeal MVA pathway is also characterized by its lower ATP consumption compared to the other MVA pathways ( Hayakawa et al, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

A [4Fe-4S] cluster resides at the active center of phosphomevalonate dehydratase, a key enzyme in the archaeal modified mevalonate pathway

et al. 2023

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The recent discovery of the archaeal modified mevalonate pathway revealed that the fundamental units for isoprenoid biosynthesis (isopentenyl diphosphate and dimethylallyl diphosphate) are biosynthesized via a specific intermediate, trans-anhydromevalonate phosphate. In this biosynthetic pathway, which is unique to archaea, the formation of trans-anhydromevalonate phosphate from (R)-mevalonate 5-phosphate is catalyzed by a key enzyme, phosphomevalonate dehydratase. This archaea-specific enzyme belongs to the aconitase X family within the aconitase superfamily, along with bacterial homologs involved in hydroxyproline metabolism. Although an iron–sulfur cluster is thought to exist in phosphomevalonate dehydratase and is believed to be responsible for the catalytic mechanism of the enzyme, the structure and role of this cluster have not been well characterized. Here, we reconstructed the iron–sulfur cluster of phosphomevalonate dehydratase from the hyperthermophilic archaeon Aeropyrum pernix to perform biochemical characterization and kinetic analysis of the enzyme. Electron paramagnetic resonance, iron quantification, and mutagenic studies of the enzyme demonstrated that three conserved cysteine residues coordinate a [4Fe-4S] cluster—as is typical in aconitase superfamily hydratases/dehydratases, in contrast to bacterial aconitase X-family enzymes, which have been reported to harbor a [2Fe-2S] cluster.

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Crystal structure of mevalonate 3,5-bisphosphate decarboxylase reveals insight into the evolution of decarboxylases in the mevalonate metabolic pathways

Cited by 6 publications

References 42 publications

Expanded Archaeal Genomes Shed New Light on the Evolution of Isoprenoid Biosynthesis

Expanded Archaeal Genomes Shed New Light on the Evolution of Isoprenoid Biosynthesis

Advances in the Synthesis and Analysis of Biologically Active Phosphometabolites

A [4Fe-4S] cluster resides at the active center of phosphomevalonate dehydratase, a key enzyme in the archaeal modified mevalonate pathway

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