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Santiago-Frangos, A.

Publications and source records attributed to Santiago-Frangos, A..

6 recordsLinked to original sources

The bacterial antiphage protein Tiamat is an ATPase and DNase whose homologs are found across the tree of life

Bacteria and archaea encode hundreds of antiviral defense systems, some with homologs found in eukaryotic innate immunity. GHL ATPases like plant MORCs and prokaryotic Tiamat defend against viruses and phage, though their architecture and biochemical activities have remained unclear. Searching thousands of proteomes, we find Tiamat is rare in prokaryotes yet enriched across eukaryotes, including green plants, aquatic chordates, sponges, placozoans, and water molds. We resolve the central DUF3684 and flanking region into three predicted folds (TPR-like repeats, an uncharacterized conserved fold, and an inactive metalloprotease-like fold) that occupy the substrate-binding position of other GHL proteins. We show that purified Bacillus cereus Tiamat hydrolyzes ATP, inefficiently nicks duplex DNA, and cleaves single-stranded DNA site-specifically. We identify Tiamat-like proteins whose C-terminal nuclease is often swapped for helicases, peptidases, or other effectors. Additionally, we show Tiamat genes neighbor helicases, DNA methyltransferases, and nucleases, suggesting some Tiamats degrade foreign nucleic acid within a multi-component complex. Eukaryotic Tiamat homologs like the close Arabidopsis homolog NO VEIN and the distant human homolog SACSIN have acquired critical non-defense roles, leaving open whether these homologs remain antiviral or have been exapted.

biochemistry↗

Structures reveal how the Cas1-2/3 integrase captures, delivers, and integrates foreign DNA into CRISPR loci

Cas1 and Cas2 are the hallmark proteins of prokaryotic adaptive immunity. However, these two proteins are often fused to other proteins and the functional association of these fusions often remain poorly understood. Here we purify Cas1 and the Cas2/3 fusion protein from Pseudomonas aeruginosa. We determine multiple structures of the Cas1-2/3 complex at distinct stages of CRISPR adaptation. Collectively, these structures reveal a prominent, positively charged channel on one face of the integration complex that captures short fragments of foreign DNA. Foreign DNA binding triggers conformational changes in Cas2/3 that expose new DNA binding surfaces necessary for homing the DNA-bound integrase to specific CRISPR loci. The length of the foreign DNA substrate determines if Cas1-2/3 docks completely onto the CRISPR repeat to successfully catalyze two sequential transesterification reactions required for integration. Taken together, these structures clarify how the Cas1-2/3 proteins orchestrate foreign DNA capture, site-specific delivery, and integration of new DNA into the bacterial genome. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/658980v1_ufig1.gif" ALT="Figure 1"> View larger version (53K): org.highwire.dtl.DTLVardef@11ad39borg.highwire.dtl.DTLVardef@3a8474org.highwire.dtl.DTLVardef@1cdf25borg.highwire.dtl.DTLVardef@1e24ff5_HPS_FORMAT_FIGEXP M_FIG C_FIG HIGHLIGHTS- A positively charged channel on the Cas1-2/3 complex captures fragments of DNA - A loop in the RecA1 domain controls access to the Cas3 nuclease active site - Foreign DNA binding allosterically regulates access to additional DNA binding sites - Distortion of the CRISPR repeat sequence licenses complete foreign DNA integration

molecular biology↗

Characterization and genomic analysis of the Lyme disease spirochete bacteriophage phiBB-1

Lyme disease is a tick-borne infection caused by the spirochete Borrelia (Borreliella) burgdorferi. Borrelia species have highly fragmented genomes composed of a linear chromosome and a constellation of linear and circular plasmids some of which are required throughout the enzootic cycle. Included in this plasmid repertoire by almost all Lyme disease spirochetes are the 32-kb circular plasmid cp32 prophages that are capable of lytic replication to produce infectious virions called {phi}BB-1. While the B. burgdorferi genome contains evidence of horizontal transfer, the mechanisms of gene transfer between strains remain unclear. While we know that {phi}BB-1 transduces cp32 and shuttle vector DNA during in vitro cultivation, the extent of {phi}BB-1 DNA transfer is not clear. Herein, we use proteomics and long-read sequencing to further characterize {phi}BB-1 virions. Our studies identified the cp32 pac region and revealed that {phi}BB-1 packages linear cp32s via a headful mechanism with preferentially packaging of plasmids containing the cp32 pac region. Additionally, we find {phi}BB-1 packages fragments of the linear chromosome and full-length plasmids including lp54, cp26, and others. Furthermore, sequencing of {phi}BB-1 packaged DNA allowed us to resolve the covalently closed hairpin telomeres for the linear B. burgdorferi chromosome and most linear plasmids in strain CA-11.2A. Collectively, our results shed light on the biology of the ubiquitous {phi}BB-1 phage and further implicates {phi}BB-1 in the generalized transduction of diverse genes and the maintenance of genetic diversity in Lyme disease spirochetes.

microbiology↗

Viral proteins activate PARIS-mediated tRNA degradation and viral tRNAs rescue infection

Viruses compete with each other for limited cellular resources, and some viruses deliver defense mechanisms that protect the host from competing genetic parasites. PARIS is a defense system, often encoded in viral genomes, that is composed of a 53 kDa ABC ATPase (AriA) and a 35 kDa TOPRIM nuclease (AriB). Here we show that AriA and AriB assemble into a 425 kDa supramolecular immune complex. We use cryo-EM to determine the structure of this complex which explains how six molecules of AriA assemble into a propeller-shaped scaffold that coordinates three subunits of AriB. ATP-dependent detection of foreign proteins triggers the release of AriB, which assembles into a homodimeric nuclease that blocks infection by cleaving the host tRNALys. Phage T5 subverts PARIS immunity through expression of a tRNALys variant that prevents PARIS-mediated cleavage, and thereby restores viral infection. Collectively, these data explain how AriA functions as an ATP-dependent sensor that detects viral proteins and activates the AriB toxin. PARIS is one of an emerging set of immune systems that form macromolecular complexes for the recognition of foreign proteins, rather than foreign nucleic acids.

biochemistry↗

Protein-mediated genome folding allosterically enhances site-specific integration of foreign DNA into CRISPRs

Bacteria and archaea acquire resistance to viruses and plasmids by integrating fragments of foreign DNA into the first repeat of a CRISPR array. However, the mechanism of site-specific integration remains poorly understood. Here, we determine a 560 kDa integration complex structure that explains how Cas (Cas1-2/3) and non-Cas proteins (IHF) fold 150 base-pairs of host DNA into a U-shaped bend and a loop that protrude from Cas1-2/3 at right angles. The U-shaped bend traps foreign DNA on one face of the Cas1-2/3 integrase, while the loop places the first CRISPR repeat in the Cas1 active site. Both Cas3s rotate 100-degrees to expose DNA binding sites on either side of the Cas2 homodimer, that each bind an inverted repeat motif in the leader. Leader sequence motifs direct Cas1-2/3-mediated integration to diverse repeat sequences that have a 5-GT.

biochemistry↗

Structure reveals mechanism of CRISPR RNA-guided nuclease recruitment and anti-CRISPR viral mimicry

Bacteria and archaea have evolved sophisticated adaptive immune systems that rely on CRISPR RNA (crRNA)-guided detection and nuclease-mediated elimination of invading nucleic acids. Here we present the cryo-EM structure of the type I-F CRISPR RNA-guided surveillance complex (Csy complex) from Pseudomonas aeruginosa bound to a double-stranded DNA target. Comparison of this structure to previously determined structures of this complex reveals a I180-degree rotation of the C-terminal helical bundle on the \"large\" Cas8f subunit. We show that the dsDNA-induced conformational change in Cas8f exposes a Cas2/3 \"nuclease recruitment helix\" that is structurally homologous to a virally encoded anti-CRISPR protein (AcrIF3). Structural homology between Cas8f and AcrIF3 suggests that AcrIF3 is a mimic of the Cas8f \"nuclease recruitment helix\", implying that cas genes may sometimes serve as genetic fodder for the evolution of anti-CRISPRs.

molecular biology↗