Implications for rational classification of recombination/repair systems, Streptomyces lividans 66 contains a gene for phage resistance which is similar to the phage lambda ea59 endonuclease gene, A novel endonuclease specified by bacteriophage lambda. (iii) Within the core P-loop domain, all ABCs have an insert between H1 and S2, which we term insert-1; it varies considerably in length and structural elaboration (Figure 1B). In this proposal, the conformational change transmitted by the ABC ATPase would result in an unfurling and activation of the effector. Thus, certain ABC ATPases have been recruited independently on several occasions to similar functional themes. Rather, they resemble the recently described nucleotide-regulated effector systems where diverse effectors are coupled to the sensing of nucleotide signals (152). Curr. Structural depictions of ABC-ATPase showing: (A)head-to-head dimeric interface (PDB ID: 5X40). The components of the SUF system include a two-subunit cysteine desulfurase complex of SufS (a pyridoxal 5-phosphate-dependent desulfurase), the sulfur shuttle protein SufE (54,55), the homologous parallel- helix domain subunits, SufB and SufD (14) and the ABC-ATPase SufC (56). Strands and helices forming the core of ASCE P-Loop NTPase domain are numbered and colored. While the three-step reaction cycle of the ABC ATPases broadly resembles other members of the ASCE clade it also shows some unique features. Pyrimidines are heterocyclic amines with two nitrogen atoms in a six-member ring and include uracil, thymine, and cytosine. AMP. Insert-2 developed a giant insert in the form of a coiled-coil arm comprised of two anti-parallel helices, followed by 3 terminal strands (Figures 1B and3). Structure This prevents us from tying their origins to a precise temporal window; however, given the ubiquity of biological conflicts we suspect that they are likely to have emerged early (Figure 3). Garcia P.S., Gribaldo S., Py B., Barras F. Hirabayashi K., Yuda E., Tanaka N., Katayama S., Iwasaki K., Matsumoto T., Kurisu G., Outten F.W., Fukuyama K., Takahashi Y. et al. Hence, it is likely they function via distinct interactions mediated by the C-terminal coiled-coil region. A characteristic feature of this complex is its structural reorganization in conjunction with end-recognition which results in the Mre11 dimer being positioned to process the DNA end (118). Their radiation primarily in a DNA-related context suggests that this probably went together with the energy-intensive processes associated with DNA as the primary genetic material, such as unwinding of dsDNA, looping of DNA for compact packaging and bridging of DNA-ends during recombination. a chlamydial endosymbiont) (68,69). Further, among the ABC ATPases the ancestral MutS, Zn-hook, and SMC clades (total of 3) are inferred as performing DNA-related functions (Figure 3). We present a unified mechanism for ABC ATPase function across disparate systems like RNA editing, translation, metabolism, DNA repair, and biological conflicts, and some unexpected recruitments, such as MutS ATPases in secondary metabolism. active transport across the lipid bilayer, the key event which allowed cells to actively acquire nutrients, deliver toxin weaponry and extrude deleterious xenobiotics. Mardenborough Y.S.N., Nitsenko K., Laffeber C., Duboc C., Sahin E., Quessada-Vial A., Winterwerp H.H.K., Sixma T.K., Kanaar R., Friedhoff P. et al. PrrC is genomically linked to the Type Ic R-M system PrrI, whose three core RM components (hsdMSR) negatively regulate the PrrC by keeping it catalytically inactive (154,160,214). Given that DndE is a non-specific DNA-binding protein, based on the precedence of other members of the coiled-coil clade such as the SMCs, which operate along with non-specific DNA-binding partners such as the kleisins and ScpB (Figure 5Q), we propose that ABC-ATPase-DndE complex forms a similar DNA-manipulating complex. The MutS clade is widely distributed across the three superkingdoms of life and certain nucleocytoplasmic large DNA viruses infecting unicellular eukaryotes. In contrast, the ASCE division to which the ABC ATPases belong is characterized by (i) an additional strand in the core sheet between the P-loop strand and the Walker B strand; (ii) a conserved proton-abstracting acidic residue (usually glutamate) which primes a water molecule for the nucleophilic attack on the -phosphate group of ATP (3,5). Travis B., Shaw P.L.R., Liu B., Ravindra K., Iliff H., Al-Hashimi H.M., Schumacher M.A. This together with the mode of ATP-binding by the barrelized -sheet facilitates an ATPase work-cycle that results in translational motion (Figure 2B). Cycling between ADP and ATP during cellular respiration gives cells the energy needed to carry out cellular activities. Consistent with this, we find multiple instances of a second RNase component such as a second HEPN or Schlafen domain in these systems. Some of these roles include (i) toxic effectors (e.g. et al. Schiltz C.J., Lee A., Partlow E.A., Hosford C.J., Chappie J.S. The monomer of nucleic acids is called a nucleotide, which is made up of a five-carbon sugar, a base, and a phosphate group. Interestingly, these systems lack a direct homolog of the DndD or CxC clade ABC ATPases; instead, we find that the ABC ATPase has been displaced by an ATPase with a distinct C-terminal domain, sspC, belonging to the STAND-Orc-CDC6 clade of AAA+ NTPases. 4. In the dimer, the interaction of hinge-I and -II from opposite monomers allows it to assume a doughnut-shaped structure with the hinges forming two eight-stranded -sheets (Figure 4A, left). PrrC and RloC (154,155,159161). This system repairs ssDNA gaps that might arise from incomplete DNA replication on faulty templates (reviewed in (107,108)) by facilitating recombination (109). Hence, this clade of unrelated ATPases has likely convergently evolved the capacity to transduce mechanical work in a manner similar to the ABC ATPases. The bacterial NER system is comprised of the UvrABC complex containing the UvrA ABC ATPase, the UvrB SF-2 helicase and UvrC with two distinct endonuclease domains. Wilkinson M., Drabavicius G., Silanskas A., Gasiunas G., Siksnys V., Wigley D.B. These systems may act as backups in the event of failure of the main effector system. Hence, it cannot be ruled out that Csn2 additionally plays such a sensory role in the type-II CRISPR/Cas systems. While across these roles the ABC ATPases utilize a strongly conserved work cycle, they have been recruited to different biological functions through combination with other domains in the same polypeptide or independent functional partners. (A)Topological diagrams showing the differences between the SMC hinge domains and the MukB. (A)Topology diagrams depicting the major divisions of the P-loop NTPases and accompanying cladogram depicting higher-order relationships. Each nucleotide is made of one of the five nitrogenous bases, a pentose sugar (ribose or deoxyribose) and a phosphate group. These are likely counterparts of the ABC ATPase+HEPN systems, where the ABC ATPase+PHP gene is embedded in bona fide Type I-like R-M systems (Figure 7B). Several distinct clades of the HEPN superfamily of RNase domains are found fused to ABC ATPases. 3. Yang Y., Xu G., Liang J., He Y., Xiong L., Li H., Bartlett D., Deng Z., Wang Z., Xiao X. Yao P., Liu Y., Wang C., Lan W., Wang C., Cao C. Zaremba M., Toliusis P., Grigaitis R., Manakova E., Silanskas A., Tamulaitiene G., Szczelkun M.D., Siksnys V., Tamulaitiene G., Silanskas A. et al. Given the rising value of enzymes from biological conflict systems as potential biotechnological reagents, we believe that the systems reported here are likely to provide further opportunities in this regard. We briefly discuss below the functional aspects of the multiple recruitments of ABC ATPases to ribonucleoprotein complexes and the notable evolutionary aspects of their radiation in this context. Nucleotides are monomers (small molecules) that are the building blocks of nucleic acids. In either case, such double-nuclease action can considerably limit repair, especially of the targeted RNAs by ligation (155). We did not detect a relationship of these to any other previously characterized domains. In other cases, they have captured different functional niches within the same general functional theme such as translation termination. This was followed by the eukaryotes acquiring two copies of this family, potentially via the alphaproteobacterial mitochondrial progenitor, which then persisted as GCN20 and Arb1. A key feature of these systems is an extraordinary array of regulatory components that either prevent the premature deployment of the effectors or their deployment against self-targets or their recycling after deployment. In the second step, the proton transfer from the catalytic glutamate to the freed -phosphate yields H2PO4 and resets the general base. The diversity in the first multidomain component is primarily in the variable N-terminal domain, which we predict to be the effector module of the system. in cyanobacteria, proteobacteria, spirochaetes, thermobaculum, and chloroflexi) the transferred Rad50Mre11 element additionally includes genes for the HerANurA dyad suggesting that a complex similar to that in archaea is also formed in the bacteria with these genes. Other less conserved associations might extend this operonic linkage to include the ArgR-family of HTH domains and a Nudix phosphoesterase also implicated in NAD+ processing (Figure 5K). Kim J.S., Shin D.H., Pufan R., Huang C., Yokota H., Kim R., Kim S.H. . Together, these examples indicate that in addition to or in place of the attack on nucleic acids, the line of defense mediated by the ABC ATPases might also trigger responses via linked effectors, which might include a suicidal attack on the cell-membrane or phosphorylation of particular substrates. Several FeS cluster proteins are part of the electron transport chain and operate close to membranes. These proteins are likely involved in the SAM, PLP and AdoCbl-dependent synthesis of an amino acid (likely lysine)-derived metabolite where the GTPase acts as a metallochaperone for loading the B12 cofactor on to the subunit of the lysine 5,6-aminomutase. Nucleic acids are made of biopolymers, which are naturally-occurring, repeated sets of monomers (making polymers) that then create nucleotides, which form nucleic acids. A single ABC ATPase is confidently inferred as functioning in a translation-associated RNA-related context, while the second one, the RNA-ABC, might have performed an RNA-related role in the more inclusive reconstruction of the LUCA complement. MukB shows an operonic association with two other genes MukE and MukF which code for wHTH domain proteins and function as partners of MukB (143,144) analogous to the kleisins and ScpB (145,146) (Figure 5R). Adenosine 5'-triphosphate, or ATP, is the principal molecule for storing and transferring energy in cells. Groothuizen F.S., Winkler I., Cristovao M., Fish A., Winterwerp H.H., Reumer A., Marx A.D., Hermans N., Nicholls R.A., Murshudov G.N. This work is written by (a) US Government employee(s) and is in the public domain in the US. These include ATPases such as the MORCs, para-MORCs and MutL. The recently solved crystal structure of Csn2 confirmed our proposal that Csn2 is an ABC ATPase, which specifically belongs to the coiled-coil clade (Figure 3) (165,169). Each nucleotide, and consists of 3 portions: pentose sugar (ribose) one or more phosphate groups one of five cyclic nitrogenous bases Nucleotides are the monomers that make up the nucleic acid polymers. Xiong L., Liu S., Chen S., Xiao Y., Zhu B., Gao Y., Zhang Y., Chen B., Luo J., Deng Z. et al. The -hairpin from this element was incorporated into the barrelized sheet of the ABC P-loop domain (Figure 1B). Further, the related CxC clade of ABC ATPases also shows a comparable linkage to a gene coding for a DndE homolog. In these systems, the ABC ATPase is fused to a C-terminal RNase domain of the HEPN superfamily (209213) (Figures 3, 7A) which targets the anticodon loops of tRNAs. None declared. After adding further eGFP-gp16, pRNA, gp9-14 and ATP, the partially filled procapsids . OLD by the coliphage P2 and Burkholderia phage KS5 (200) and E59 by (201,202). The version of the domain in RNA-ABC and one of the two ATPase domains of the EttA-like families, UVRA, EF3 and RLI-1 (21,22,27,48) are also relatively close to the inferred primitive state (Figure 3). Further, in eukaryotes certain MORCs have fused with the SMC hinge domains and a coiled-coil to generate a configuration equivalent to the SMCs (193). Notably, MukB and its partners are faster evolving relative to the SMCs and show degeneration of one of two copies of the Hinge domain in their hinge regions (Figure 4A). Further, it is distinguished by the fusion to an N-terminal iron-sulfur (4Fe4S)-cluster-binding ferredoxin domain (Figures 3, 5C) that has been recruited for an unusual role. SufC and likely a single ancestral ABC transporter can be inferred as being present in the LUCA (Figure 3). 1. monosaccharides, simple sugars 2. glucose is a monosaccharide central carbon atom covalently bonded to 4 groups of atoms a) amino group (NH_2) b) carboxyl group (COOH) c) hydrogen (H) d) the functional group (R) D. disaccharides 1. maltose, sucrose, lactose 2. Sigma factors and the selectivity of transcription initiation in bacteria, MutS2 promotes homologous recombination in bacillus subtilis, The multicatalytic compartment of propionyl-CoA synthase sequesters a toxic metabolite, A switch III motif relays signaling between a B12 enzyme and its G-protein chaperone, Crystal structures of Mycobacterial MeaB and MMAA-like GTPases, A locking mechanism preventing radical damage in the absence of substrate, as revealed by the x-ray structure of lysine 5,6-aminomutase, Large-scale domain motions and pyridoxal-5-phosphate assisted radical catalysis in coenzyme B12-dependent aminomutases, The evolution and mechanisms of nucleotide excision repair proteins, Unexpected evolution of lesion-recognition modules in eukaryotic NER and Kinetoplast DNA dynamics proteins from bacterial mobile elements, The biological and structural characterization of Mycobacterium tuberculosis UvrA provides novel insights into its mechanism of action, Sources of DNA double-strand breaks and models of recombinational DNA repair, The cohesin-like RecN protein stimulates RecA-mediated recombinational repair of DNA double-strand breaks, Double-strand break repair in bacteria: a view from Bacillus subtilis, Comparative and evolutionary analysis of the bacterial homologous recombination systems, Single-strand gap repair involves both RecF and RecBCD pathways, DNA ADP-ribosylation stalls replication and is reversed by RecF-mediated homologous recombination and nucleotide excision repair, DciA is an ancestral replicative helicase operator essential for bacterial replication initiation, Substrate binding analysis of the 23S rRNA methyltransferase RrmJ, Structural and functional properties of NAD kinase, a key enzyme in NADP biosynthesis, Homologous recombination and the formation of complex genomic rearrangements, Non-homologous DNA end joining and alternative pathways to double-strand break repair, Phosphoesterase domains associated with DNA polymerases of diverse origins, 20 Years of Mre11 biology: no end in sight, Mechanism of DNA end sensing and processing by the Mre11-Rad50 complex, SbcC-SbcD and ExoI process convergent forks to complete chromosome replication, RecBCD enzyme and the repair of double-stranded DNA breaks, Mechanistic insight into the assembly of the HerA-NurA helicase-nuclease DNA end resection complex, Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52, RecE/RecT and Redalpha/Redbeta initiate double-stranded break repair by specifically interacting with their respective partners, Sak4 of phage HK620 is a RecA remote homolog with single-strand annealing activity stimulated by its cognate SSB protein, SURVEY AND SUMMARY: holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories, Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging, Nucleases of the metallo-beta-lactamase family and their role in DNA and RNA metabolism, Diversity and evolution of chromatin proteins encoded by DNA viruses, Towards a unified model of SMC complex function, At the heart of the chromosome: SMC proteins in action, SMC complexes organize the bacterial chromosome by lengthwise compaction, Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners, The structure of the cohesin ATPase elucidates the mechanism of SMC-kleisin ring opening, Discovery of two novel families of proteins that are proposed to interact with prokaryotic SMC proteins, and characterization of the Bacillus subtilis family members ScpA and ScpB, Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein, Crystal structure of ScpB from Chlorobium tepidum, a protein involved in chromosome partitioning, Cloning, expression, purification, crystallization and X-ray crystallographic analysis of ScpB (Rv1710) from Mycobacterium tuberculosis. Implications for ATP hydrolysis and conformational changes, Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily, Structural basis for allosteric cross-talk between the asymmetric nucleotide binding sites of a heterodimeric ABC exporter, A vocabulary of ancient peptides at the origin of folded proteins, The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch, Evolutionary convergence and divergence in archaeal chromosomal proteins and Chromo-like domains from bacteria and eukaryotes, Molecular architecture of SMC proteins and the yeast cohesin complex, Crystal structure of the MukB hinge domain with coiled-coil stretches and its functional implications, Structure and mechanism of the UvrA-UvrB DNA damage sensor, The plastidial Arabidopsis thaliana NFU1 protein binds and delivers [4Fe-4S] clusters to specific client proteins, Biogenesis of Fe-S cluster by the bacterial Suf system: SufS and SufE form a new type of cysteine desulfurase, Mechanistic studies of the SufS-SufE cysteine desulfurase: evidence for sulfur transfer from SufS to SufE, SufC: an unorthodox cytoplasmic ABC/ATPase required for [Fe-S] biogenesis under oxidative stress, Native Escherichia coli SufA, coexpressed with SufBCDSE, purifies as a [2Fe-2S] protein and acts as an Fe-S transporter to Fe-S target enzymes, The SufBCD Fe-S scaffold complex interacts with SufA for Fe-S cluster transfer, Atomic resolution structures of rieske iron-sulfur protein: role of hydrogen bonds in tuning the redox potential of iron-sulfur clusters, The RAGNYA fold: a novel fold with multiple topological variants found in functionally diverse nucleic acid, nucleotide and peptide-binding proteins, The RRM of the kRNA-editing protein TbRGG2 uses multiple surfaces to bind and remodel RNA, Tying up loose ends: ribosome recycling in eukaryotes and archaea, Structural insights into the mammalian late-stage initiation complexes, The origin and evolution of release factors: implications for translation termination, ribosome rescue, and quality control pathways, Molecular analysis of the ribosome recycling factor ABCE1 bound to the 30S post-splitting complex, Control of mRNA translation by versatile ATP-Driven machines, Regulatory potential, phyletic distribution and evolution of ancient, intracellular small-molecule-binding domains, Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids, The endosymbiotic origin, diversification and fate of plastids. The P-loop NTPase fold is a three-layered / sandwich containing regularly recurring - units with the -strands forming a central, mostly parallel sheet, which is sandwiched between -helices on both sides (25) (Figure 1A). Curr. The first of these is one of the basal branches of the ABC superfamily, the RNA-ABC. These observations suggest that like the cellular coiled-coil ABC ATPases (SbcC/Rad50) or their phage counterparts (see above), the Csn2 marks and possibly bridges double-strand breaks for repair. In archaea, the Rad50Mre11 system shows a genomic linkage to the genes coding for the ATPase HerA and the nuclease NurA that generate 3 overhangs in DNA required for the subsequent repair steps (121) (Figure 5M). Nucleic acids contain the same elements as proteins: carbon, hydrogen, oxygen, nitrogen; plus phosphorous (C, H, O, N, and P). Gene neighborhoods are depicted as box arrows with the multiple domains in each product individually colored. The PHP domains are TIM-barrel fold phosphoesterases, versions of which also cleave nucleic acids (191,192). Other examples of the above systems also show characteristic features of DNA-targeting enzymes such as the RHH DNA-binding domain found in systems with the URI endonuclease, or the HNH+ParB combination related to type IV RM systems, versions of which have been shown to cleave DNA (216218). (C)Phyletic patterns of the families within the ABC ATPase superfamily color-coded according to the percentage of representation within the specified taxa. This clamp then recruits MutL to form the MutS-MutL complex that mediates strand discrimination followed by an endonucleolytic cut either via a standalone endonuclease (e.g. The host might either be able to tide over such inhibition as a period of dormancy (a known defense mechanism against phages (220), or if it undergoes suicide it can preempt viral spread to kin cells or other cells in a multicellular assemblage (154,155,159161). Adenosine triphosphate (ATP) is a nucleotide that has an important function by itself. Likewise, the E59 (Early59, abbreviated as Ea59 or E59), originally identified in phage , is implicated in inter-phage conflict and bacterial counter-phage defense mechanisms (201203). The three translation factors, Arb1, GCN20 and eEF3, form a distinct family within the translation clade with ribosome-associated functions (Figure 3). Of these, DciA has the most widespread association with RecF found across various bacterial lineages, while S4 and DUF370 were more restricted (Supplementary Material). The elaboration of insert-2 also provided an interface for the interaction with target proteins or nucleic acids in conjunction with the helical region in insert-1. We also observe instances of clustering of multiple copies of these antibiotic resistance families on the genome (Figure 5E). The last category spans the entire range of interactions from hostparasite to predator-prey interactions. To objectively define the distinctive features of the ABC ATPases we collated structures of all known representatives of the ABC clade and used them as queries to run DALI searches against the Protein Data Bank (PDB) database. However, some roles, like transmembrane transport, have remained more or less fixed since the earliest period of their appearance. . firmicutes and actinobacteria in the bacterial superkingdom. Unlike PrrC, the RloC is not linked to the RM systems and its HEPN RNase domain is kept inactive by its N-terminal ABC-ATPase domain under normal conditions. This helical element forms a major binding interface for either partner proteins (e.g. This complex might be utilized both in the DNA-modifying Dnd system as well as the below systems which we uncovered for the first time in this study. This energy can be temporarily held on ATP molecules in the covalent bonds formed between free phosphate groups and adenosine diphosphate (ADP). EttA regulates translation by binding the ribosomal E site and restricting ribosome-tRNA dynamics, ABCF ATPases involved in protein synthesis, ribosome assembly and antibiotic resistance: structural and functional diversification across the tree of life, ABC-F proteins mediate antibiotic resistance through ribosomal protection, Resistance to telithromycin is conferred by msr(A), msrC and msr(D) in Staphylococcus aureus, An Enterococcus faecalis ABC homologue (Lsa) is required for the resistance of this species to clindamycin and quinupristin-dalfopristin, A new evolutionary variant of the streptogramin A resistance protein, Vga(A)LC, from Staphylococcus haemolyticus with shifted substrate specificity towards lincosamides, Characterization of sal(A), a novel gene responsible for lincosamide and streptogramin A resistance in Staphylococcus sciuri, Structural basis for antibiotic resistance mediated by the Bacillus subtilis ABCF ATPase VmlR, Cloning of aminoglycoside phosphotransferase (APH) gene from antibiotic-producing strain of Bacillus circulans into a high-expression vector, pKK223-3. They underwent distinct phases of structural innovation with the emergence of inserts constituting conserved binding interfaces for proteins or nucleic acids and the adoption of a unique dimeric toroidal configuration for DNA-threading. Unlike the above versions, these occur in a conserved six-gene locus found in certain bacteroidetes, elusimicrobia, tenericutes, thermotogae, proteobacteria and firmicutes. Besides this, RLI also engages the 30S post-splitting complex participating in the subsequent steps of ribosome recycling (65). Within these gene-neighborhoods, Csn2 is specifically linked to Cas1Cas2 with a strong preserved Cas1-Cas2-Csn2 gene order (Figure 6A). Chang H.H.Y., Pannunzio N.R., Adachi N., Lieber M.R. Further, the DnaG primase might initiate re-synthesis of the DNA during lesion repair. Complex assembly and origin activation requires DnaA-ATP, which differs from DnaA-ADP in its ability to cooperatively bind specific low affinity sites and also to oligomerize into helical filaments. Its phyletic distribution is comparable to RecF indeed, both RecF and RecN might have emerged via a duplication event from a common precursor in the ancestral bacterium (Figure 3). The next split marks the separation of the RNA-ABC ATPase, which like MutS, lacks any major developments in insert-1 and the glutamine downstream of S2 (Figure 3, Supplementary Tables S1 and S2, Data).
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