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Modified Mevalonate Pathway of the Archaeon Aeropyrum Pernix Proceeds Via Trans- Anhydromevalonate 5-Phosphate

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Modified Mevalonate Pathway of the Archaeon Aeropyrum Pernix Proceeds Via Trans- Anhydromevalonate 5-Phosphate Modified mevalonate pathway of the archaeon Aeropyrum pernix proceeds via trans- anhydromevalonate 5-phosphate Hajime Hayakawaa, Kento Motoyamaa, Fumiaki Sobuea, Tomokazu Itoa, Hiroshi Kawaideb, Tohru Yoshimuraa, and Hisashi Hemmia,1 aDepartment of Applied Molecular Bioscience, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, 464-8601 Aichi, Japan; and bInstitute of Symbiotic Science and Technology, Tokyo University of Agriculture and Technology, Fuchu, 183-8509 Tokyo, Japan Edited by C. Dale Poulter, University of Utah, Salt Lake City, UT, and approved August 23, 2018 (received for review May 28, 2018) The modified mevalonate pathway is believed to be the upstream MVA pathway exists in almost all eukaryotes and in certain forms biosynthetic route for isoprenoids in general archaea. The partially of bacteria, such as lactic acid bacteria, whereas the vast majority identified pathway has been proposed to explain a mystery of bacteria utilize the methylerythritol phosphate (MEP) pathway surrounding the lack of phosphomevalonate kinase and diphospho- that proceeds through completely different intermediates from mevalonate decarboxylase by the discovery of a conserved enzyme, those in the MVA pathway. isopentenyl phosphate kinase. Phosphomevalonate decarboxylase The “modified” MVA pathway was first proposed in 2006 by was considered to be the missing link that would fill the vacancy in Grochowski et al. (4) based on the discovery of a new enzyme, the pathway between mevalonate 5-phosphate and isopentenyl isopentenyl phosphate kinase (IPK), and on data from compar- phosphate. This enzyme was recently discovered from haloarchaea ative analyses of archaeal genomes. For archaea, which do not and certain Chroloflexi bacteria, but their enzymes are close homo- possess the MEP pathway, the MVA pathway is requisite for the logs of diphosphomevalonate decarboxylase, which are absent in biosynthesis of specific membrane lipids and other isoprenoids, most archaea. In this study, we used comparative genomic analysis to such as respiratory quinones and dolichols. These organisms do find two enzymes from a hyperthermophilic archaeon, Aeropyrum have the putative genes of most enzymes in the aforementioned pernix, that can replace phosphomevalonate decarboxylase. One en- eukaryote-type MVA pathway; it is curious, however, that almost zyme, which has been annotated as putative aconitase, catalyzes the all archaea apparently lack the genes of one or two enzymes of the pathway, typically both PMK and DMD (5–7). Thus, dehydration of mevalonate 5-phosphate to form a previously un- trans Grochowski et al. (4) proposed a bypass pathway, called the known intermediate, -anhydromevalonate 5-phosphate. Then, modified MVA pathway, in which isopentenyl phosphate (IP) another enzyme belonging to the UbiD-decarboxylase family, which was formed from MVA5P by an undiscovered decarboxylase likely requires a UbiX-like partner, converts the intermediate into iso- and was then phosphorylated by IPK, which is conserved in al- pentenyl phosphate. Their activities were confirmed by in vitro assay most all archaea, to yield IPP (Fig. 1A). The decarboxylase [i.e., with recombinant enzymes and were also detected in cell-free extract phosphomevalonate decarboxylase (PMD)] was recently identi- from A. pernix. These data distinguish the modified mevalonate path- fied from a halophilic archaeon, Haloferax volcanii (8), and a way of A. pernix and likely, of the majority of archaea from all known Chloroflexi bacterium, Roseiflexus castenholzii (9). The discovery mevalonate pathways, such as the eukaryote-type classical pathway, substantiated the existence of the proposed modified pathway in the haloarchaea-type modified pathway, and another modified path- these organisms. The pathway is, however, considered to be ex- way recently discovered from Thermoplasma acidophilum. ceptional in the domain Archaea, because the gene of PMD, mevalonate pathway | archaea | isoprenoid | dehydratase | decarboxylase Significance he mevalonate (MVA) pathway provides fundamental pre- Herein, the partially identified “modified” mevalonate path- Tcursors for isoprenoid biosyntheses, such as isopentenyl di- way of the majority of archaea is elucidated using information phosphate (IPP) and dimethylallyl diphosphate (DMAPP). This from comparative genomic analysis. Discovery of two enzymes, pathway was discovered in the late 1950s through the study of mevalonate 5-phosphate dehydratase and trans-anhydromevalonate cholesterol biosynthesis (Fig. 1A) (1, 2). In this pathway, the C6 5-phosphate decarboxylase, from a hyperthermophilic archaeon, intermediate MVA is formed from acetyl-CoA via acetoacetyl- Aeropyrum pernix, shows that the pathway passes through a CoA and hydroxymethylglutaryl-CoA. It then undergoes two previously unrecognized metabolite, trans-anhydromevalonate steps of phosphorylation catalyzed by mevalonate kinase (MVK) 5-phosphate. The distribution of the known mevalonate path- and phosphomevalonate kinase (PMK) to yield mevalonate 5- ways among archaea and other organisms suggests that the A. diphosphate (MVA5PP) via mevalonate 5-phosphate (MVA5P). pernix-type pathway, which is probably conserved among the The C5 compound IPP is synthesized by the decarboxylation of majority of archaea, is the evolutionary prototype for the other MVA5PP accompanied by a detachment of its 3-hydroxyl group. mevalonate pathways involving diphosphomevalonate decar- To catalyze the reaction, diphosphomevalonate decarboxylase boxylase or its homologs. (DMD) consumes ATP to temporarily phosphorylate MVA5PP and form mevalonate 3-phosphate 5-diphosphate inside its cat- Author contributions: T.Y. and H. Hemmi designed research; H. Hayakawa, K.M., F.S., T.I., alytic pocket as shown recently by our mutagenic study (3). H.K., and H. Hemmi performed research; H.K. contributed new reagents/analytic tools; Detachment of the 3-phosphate group of the intermediate triggers H. Hayakawa, F.S., and H. Hemmi analyzed data; and H. Hemmi wrote the paper. decarboxylation to yield IPP. These ATP-dependent enzymes, The authors declare no conflict of interest. MVK, PMK, and DMD, belong to the GHMP (galactokinase, This article is a PNAS Direct Submission. homoserine kinase, mevalonate kinase, phosphomevalonate ki- Published under the PNAS license. nase) kinase family and show a certain level of homology. Con- 1To whom correspondence should be addressed. Email: [email protected]. version of IPP into DMAPP is catalyzed by IPP isomerase, which This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. includes two evolutionary independent types of enzymes. This 1073/pnas.1809154115/-/DCSupplemental. most widely accepted, sometimes called “classical” or “canonical,” Published online September 17, 2018. 10034–10039 | PNAS | October 2, 2018 | vol. 115 | no. 40 www.pnas.org/cgi/doi/10.1073/pnas.1809154115 Downloaded by guest on September 27, 2021 Fig. 1. Variation and distribution of the MVA pathways. (A) The MVA pathways known to date and discovered in this study. The names of enzymes are shown in boxes, which are colored in light blue, green, or pink when the enzymes are DMD homologs. IDI, isopentenyl diphosphate isomerase. (B) Distri- bution patterns of DMD homologs and the enzymes studied in this work. Each box represents an archaeal species selected on the basis of the one-species-for- each-genus rule (SI Appendix, Table S1). Boxes colored in light blue, green, pink, and gray indicate archaea possessing the (putative) genes of DMD, PMD, M3K/BMD, and a DMD homolog of unknown function, respectively, while white boxes mean their absence. Similarly, boxes colored in red represent the presence of the putative ortholog genes of proteins described on the left. which is a close homolog to DMD, is conserved in all haloarchaea This discovery meant that the majority of archaea, in which the but not in most archaea. Different MVA pathways have been found putative orthologs of these enzymes are conserved, likely utilize from other unusual archaea that also possess DMD homologs, such the modified MVA pathway that goes via tAHMP and thus, is as those of the orders Sulfolobales and Thermoplasmatales. The distinct from the known MVA pathways. archaea of the order Sulfolobales, such as Sulfolobus solfataricus, are known to possess a eukaryote-type MVA pathway, but these Results are rare exceptions in archaea (10). In contrast, recent studies Search for Enzymes Involved in the MVA Pathway. To find candi- have proven that the archaea of the order Thermoplasmatales, dates for the undiscovered enzymes involved in the modified such as Thermoplasma acidophilum and Picrophilus torridus,pos- MVA pathway, genes conserved in the archaea that lack the sess a distinctly modified MVA pathway, in which MVA is first genes of DMD homologs were searched from the genomes of 88 converted into mevalonate 3-phosphate (MVA3P) by a DMD archaeal species using the MBGD website (mbgd.genome.ad.jp) homolog, mevalonate 3-kinase (M3K) (Fig. 1A)(11–13). MVA3P that can create sets of putative ortholog genes. The candidate is then phosphorylated by a non-GHMP family kinase, MVA3P 5- genes that we searched for were expected to be absent in the kinase, to form mevalonate 3,5-bisphosphate. The decarboxyl- archaea possessing the DMD homolog genes, such as those of ation of the intermediate is catalyzed by another DMD homolog, the class Halobacteria and the orders Sulfolobales and Ther- bisphosphomevalonate decarboxylase (BMD),
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