Radical SAM
Radical SAM is a designation for a superfamily of enzymes that use a 4Fe-4S|+ cluster to reductively cleave S-adenosyl-L-methionine to generate a radical, usually a 5′-deoxyadenosyl radical, as a critical intermediate. These enzymes utilize this potent radical intermediate to perform an array of unusual transformations, often to functionalize unactivated C-H bonds. Radical SAM enzymes are involved in cofactor biosynthesis, enzyme activation, peptide modification, post-transcriptional and post-translational modifications, metalloprotein cluster formation, tRNA modification, lipid metabolism, biosynthesis of antibiotics and natural products etc. The vast majority of known radical SAM enzymes belong to the radical SAM superfamily, and have a cysteine-rich motif that matches or resembles CxxxCxxC.
History and mechanism
As of 2001, 645 unique radical SAM enzymes have been identified from 126 species in all three domains of life. According to the EFI and SFLD databases, more than 220,000 radical SAM enzymes are predicted to be involved in 85 types of biochemical transformations.The mechanism for these reactions entail transfer of a methyl or adenosyl group from sulfur to iron. The resulting organoiron complex subsequently releases the organic radical. The latter step is reminiscent of the behavior of adenosyl and methyl cobalamins.
Nomenclature
All enzymes including radical SAM superfamily follow an easy guideline for systematic naming. Systematic naming of enzymes allows a uniform naming process that is recognized by all scientists to understand corresponding function. The first word of the enzyme name often shows the substrate of the enzyme. The position of the reaction on the substrate will also be in the beginning portion of the name. Lastly, the class of the enzyme will be described in the other half of the name which will end in suffix -ase. The class of an enzyme will describe what the enzyme is doing or changing on the substrate. For example, a ligase combines two molecules to form a new bond.and is responsible for radical generation. β-sheets are colored yellow and α-helices are shown in cyan. |alt=
Reaction classification
Representative/Prototype enzymes will only be mentioned for each reaction scheme. The audience is highly encouraged to research more into current studies on radical SAM enzymes. Many of which are responsible for fascinating yet important reactions.Radical SAM enzymes and their mechanisms known before 2008 are well-summarized by Frey et al, 2008. Since 2015, more review articles on radical SAM enzymes are open to the public. The following are only a few out of many informative resources on radical SAM enzymes.
- Recent Advances in Radical SAM Enzymology: New Structures and Mechanisms:
- Radical S-Adenosylmethionine Enzymes:
- Radical S-Adenosylmethionine Enzymes in Cofactor Biosynthesis: A Treasure Trove of Complex Organic Radical Rearrangement Reactions:
- Molecular architectures and functions of radical enzymes and their activating proteins:
Carbon methylation
Class A sub-family
- Class A enzymes methylates specific adenosine residues on rRNA and/or tRNA. In other words, they are RNA base-modifying radical SAM enzymes.
- The most mechanistically well-characterized are enzymes RlmN and Cfr. Both enzymes methylates substrate by adding a methylene fragment originating from SAM molecule. Therefore, RlmN and Cfr are considered methyl synthases instead of methyltransferases.
Class B sub-family
- Class B enzymes are the largest and most versatile which can methylate a wide range of carbon and phosphorus centers.
- These enzymes require a cobalamin cofactor as an intermediate methyl group carrier to transfer a methyl group from SAM to substrate.
- One well-investigated representative enzyme is TsrM which involves in tryptophan methylation in thiostrepton biosynthesis.
Class C sub-family
- Class C enzymes are reported to play roles in biosynthesis of complex natural products and secondary metabolites. These enzymes methylate heteroaromatic substrates and are cobalamin-independent.
- These enzymes contain both the radical SAM motif and exhibit striking sequence similarity to coproporhyrinogen III oxidase, a radical SAM enzyme involved in heme biosynthesis
- Recently, detailed mechanistic investigation on two important class C radical SAM methylases have been reported:
- # TbtI is involved in the biosynthesis of potent thiopeptide antibiotic thiomuracin.
- # Jaw5 is suggested to be responsible for cyclopropane modifications.
Class D sub-family
- Class D is the most recently discovered and has been shown to not use SAM for methylation which is different from the three classes described above. Instead, these enzymes use methylenetetrahydrofolate as the methyl donor.
- The prototype MJ0619 is proposed to play a role in the biosynthesis of cofactor methanopterin which is required in methanogesis, an essential methane-producing pathway dominantly found in the Archaean domain.
Methylthiolation of tRNAs
MiaB and RimO are both well-characterized and bacterial prototypes for tRNA-modifying methylthiotransferases
- MiaB introduces a methylthio group to the isopentenylated A37 derivatives in the tRNA of S. Typhimurium and E. coli by utilizing one SAM molecule to generate 5'-dAdo radical to activate the substrate and a second SAM to donate a sulfur atom to the substrate.
- RimO is responsible for post-translational modification of Asp88 of the ribosomal protein S12 in E. coli. A recently determined crystal structure sheds light on the mechanistic action of RimO. The enzyme catalyzes pentasulfide bridge formation linking two Fe-S clusters to allow for sulfur insertion to the substrate.
Sulfur insertion into unreactive C-H bonds
Sulfurtransferases are a small subset of radical SAM enzymes. Two well-known examples are BioB and LipA which are independently responsible for biotin synthesis and lipoic acid metabolism, respectively.- BioB or biotin synthase is a radical SAM enzyme that employs one center to thiolate dethiobitin, thus converting it to biotin or also known as vitamin B7. Vitamin B7 is a cofactor used in carboxylation, decarboxylation, and transcarboxylation reactions in many organisms.
- LipA or lipoyl synthase is radical SAM sulfurtransferase utilizing two clusters to catalyze the final step in lipoic acid biosynthesis.
Carbon insertion
Anaerobic oxidative decarboxylation
- One well-studied example is HemN. HemN or anaerobic coproporphyrinogen III oxidase is a radical SAM enzyme that catalyzes the oxidative decarboxylation of coproporphyrinogen III to protoporhyrinogen IX, an important intermediate in heme biosynthesis. A recently published study shows evidence supporting HemN utilizes two SAM molecules to mediate radical-mediated hydrogen transfer for the sequential decarboxylation of the two propionate groups of coproporphyrinogen III.
- Hyperthermophilic sulfate-reducing archaen Archaeoglobus fulgidus has been recently reported to enable anaerobic oxidation of long chain n-alkanes. PflD is reported to be responsible for the capacity of A. fulgidus to grow on a wide range of unsaturated carbons and fatty acids. A detailed biochemical and mechanistic characterization of PflD is still undergoing but preliminary data suggest PflD may be a radical SAM enzyme.
Protein radical formation
- Pyruvate formate-lyase activating enzyme catalyzes the activation of PFL, a central enzyme in anaerobic glucose metabolism in microbes.
- Benzylsuccinate synthase is a central enzyme in anaerobic toluene catabolism.
Peptide modifications
Another important subset of peptide-modifying radical SAM enzymes is SPASM/Twitch domain-carrying enzymes. SPASM/Twitch enzymes carry a functionalized C-terminal extension for the binding of two clusters, especially important in post-translational modifications of peptides.
The following examples are representative enzymes that can catalyze peptide modifications to generate specific natural products or cofactors.
- TsrM in thiostrepton biosynthesis
- PoyD and PoyC in polytheonamide biosynthesis
- TbtI in thiomuracin biosynthesis
- NosN in nosiheptide biosynthesis
- MoaA in molybdopterin biosynthesis
- PqqE in pyrroloquinoline quinone biosynthesis
- TunB in tunicamycin biosynthesis
- OxsB in oxetanocin biosynthesis
- BchE in anaerobic bacteriochlorophyll biosynthesis
- F0 synthases in F420 cofactor biosynthesis
- MqnE and MqnC in menaquinone biosynthesis
- QhpD in post-translational processing of quinohemoprotein amine dehydrogenase
Epimerization
- PoyD installs numerous D-stereocenters in enzyme PoyA to ultimately help facilitate polytheonamide biosynthesis. Polytheoamide is a natural potent cytoxic agent by forming pores in membranes. This peptide cytotoxin is naturally produced by uncultivated bacteria that exist as symbionts in a marine sponge.
- YydG epimerase modifies two amino acid positions on YydF in Gram-positive Bacillus subtilis. A recent study has reported the extrinsically added YydF mediates subsequent dissipation of membrane potential via membrane permeabilization, resulting in death of the organism.
Complex carbon skeleton rearrangements
- DNA spore photoproduct lysase is a radical SAM that can repair DNA thymine dimers caused by UV radiation. Despite of remaining unknowns and controversies involving SPL-catalyzed reaction, it is certain that SPL utilizes SAM as a cofactor to generate 5'-dAdo radical to revert SP to two thymine residues.
- HydG is a radical SAM responsible for generating CO and CN− ligands in the -hydrogenase in various anaerobic bacteria.
- Radical SAM MoaA and MoaC are involved in converting GTP into cyclic pyranopterin monophosphate. Overall, both play important roles in molybdopterin
biosynthesis. Other reactions
- A recent study has reported a novel radical SAM enzyme with intrinsic lyase activity that is able to catalyze lysine transfer reaction, generating archaea-specific archaosine-containing tRNAs.
- Viperin is an interferon-stimulated radical SAM enzyme which converts CTP to ddhCTP, which is a chain terminator for viral RdRps and therefore a natural antiviral compound.
Clinical considerations
- Deficiency in human tRNA methylthiotransferase eMtaB has been shown to be responsible for abnormal insulin synthesis and predisposition to type 2 diabetes.
- Mutations in human GTP cyclase MoaA has been reported to lead to molybdenum cofactor deficiency, a usually fatal disease accompanied by severe neurological symptoms.
- Mutations in human wybutosine-tRNA modifying enzyme Tyw1 promotes retrovirus infection.
- Alterations in human tRNA-modifying enzyme Elp3 results in progression into amyotrophic lateral sclerosis.
- Mutations in human antiviral RSAD1 has been shown to be associated with congenital heart disease.
- Mutations in human sulfurtransferase LipA has been implicated in glycine encephalopathy, pyruvate dehydrogenase and lipoic acid synthetase deficiency.
- Mutations in human methylthiotransferase MiaB are related to impaired cardiac and respiratory functions.
Therapeutic applications
- Inhibition of radical SAM enzyme MnqE in menaoquinone biosynthesis is reported to be an effective antibacterial strategy against H. pylori.
- Radical SAM enzyme BlsE has recently been discovered to be a central enzyme in blasticidin S biosynthetic pathway. Blasticidin S produced by Streptomyces griseochromogenes exhibits strong inhibitory activity against rice blast caused by Pyricularia oryzae Cavara. This compound specifically inhibits protein synthesis in both prokaryotes and eukaryotes through inhibition of peptide bond formation in the ribosome machinery.
- A new fungal radical SAM enzyme has also been recently reported to facilitate the biocatalytic routes for synthesis of 3'-deoxy nucleotides/nucleosides. 3'deoxynucleotides are an important class of drugs since they interfere with the metabolism of nucleotides, and their incorporation into DNA or RNA terminates cell division and replication. This activity explains why this compound is an essential group of antiviral, antibacterial or anticancer drug.
Examples
Radical
Examples of radical SAM enzymes found within the radical SAM superfamily include:- AblA - lysine 2,3-aminomutase
- AlbA - subtilosin maturase
- AtsB - anaerobic sulfatase activase
- BchE - anaerobic magnesium protoporphyrin-IX oxidative cyclase
- BioB - biotin synthase
- BlsE - cytosylglucuronic acid decarboxylase - blasticidin S biosynthesis
- BtrN - butirosin biosynthesis pathway oxidoreductase
- Cfr - 23S rRNA -C)-methyltransferase - rRNA modification for antibiotic resistance
- CofG - FO synthase, CofG subunit
- CofH - FO synthase, CofH subunit
- CutD - trimethylamine lyase-activating enzyme
- DarE - darobactin maturase
- DesII - D-desosamine biosynthesis deaminase
- EpmB - elongation factor P beta-lysylation protein
- HemN - oxygen-independent coproporphyrinogen III oxidase
- HmdB - 5,10-methenyltetrahydromethanopterin hydrogenase cofactor biosynthesis protein HmdB
- HpnR - hopanoid C-3 methylase
- HydE - hydrogenase H-cluster radical SAM maturase
- HydG - hydrogenase H-cluster radical SAM maturase
- LipA - lipoyl synthase
- MftC - mycofactocin system maturase
- MiaB - tRNA methylthiotransferase
- MoaA - GTP 3',8-cyclase
- MqnC - dehypoxanthine futalosine cyclase
- MqnE - aminofutalosine synthase
- NifB - cofactor biosynthesis protein NifB
- NirJ - heme d1 biosynthesis radical SAM protein NirJ
- NosL - complex rearrangement of tryptophan to 3-methyl-2-indolic acid - nosiheptide biosynthesis
- NrdG - anaerobic ribonucleoside-triphosphate reductase activase
- PflA - pyruvate formate-lyase activating enzyme
- PhpK - radical SAM P-methyltransferase - antibiotic biosynthesis
- PqqE - PQQ biosynthesis enzyme
- PylB - methylornithine synthase, pyrrolysine biosynthesis protein PylB
- QhpD - quinohemoprotein amine dehydrogenase maturation protein
- QueE - 7-carboxy-7-deazaguanine synthase
- RimO - ribosomal protein S12 methylthiotransferase
- RlmN - 23S rRNA -C)-methyltransferase
- ScfB - SCIFF maturase
- SkfB - sporulation killing factor maturase
- SplB - spore photoproduct lyase
- ThiH - thiazole biosynthesis protein ThiH
- TrnC - thuricin biosynthesis
- TrnD - thuricin biosynthesis
- TsrT - tryptophan 2-C-methyltransferase
- TYW1 - 4-demethylwyosine synthase
- YqeV - tRNA methylthiotransferase
Non-canonical
- ThiC - thiamine biosynthesis protein ThiC
- Dph2 - diphthamide biosynthesis enzyme Dph2
- PhnJ - phosphonate metabolism protein PhnJ